Cleanliness of Hands and Surfaces Plays Key Role in Cross-Contamination Prevention

By Kelly M. Pyrek

Hand-carriage of pathogens remains one of the most significant challenges in the healthcare settings because it is so pervasive and is inextricably linked to the state of cleanliness of surfaces in the patient-care environment.

Huslage, et al. (2010) remind us that, "In the global infection control community, it is widely accepted that contaminated environmental surfaces, contaminated equipment, and contaminated hands of healthcare workers all have been linked to the transmission of several pathogens, which has led to individual cases and multiple outbreaks of healthcare-acquired infection."

Frequently touched surfaces may serve as a reservoir for infectious pathogens and that these microorganisms are transmitted directly or indirectly by the hands of healthcare workers (Pittet, et al. 2006). So-called "high-touch" surfaces -- and the role that inanimate objects in the immediate vicinity of a patient play in the transmission of healthcare-associated pathogens -- have received a great deal of attention, to the point that the Healthcare Infection Control Practices Advisory Committee (HICPAC) and the Centers for Disease Control and Prevention (CDC) recommended that high-touch surfaces such as doorknobs, bed rails, light switches, and surfaces in and around toilets in patients’ rooms should be cleaned and disinfected  on a more frequent basis than minimal-touch surfaces.
However, as Huslage, et al. (2010) pointed out in their study at the time, "no one has quantitatively assessed the frequency of healthcare worker contact with different room surfaces. Similarly, the types of pathogens found on different room surfaces and their microbial load have also not been systematically evaluated. We do know that important nosocomial pathogens-including vancomycin-resistant enterococci (VRE), methicillin-resistant Staphylococcus aureus (MRSA), Acinetobacter baumannii, Clostridium difficile, Escherichia coli, and Pseudomonas aeruginosa-have been shown to persist in the environment for several days to several months."

Huslage, et al. (2010) sought to confirm the potential for purported high-touch surfaces to harbor pathogens, and to obtain a quantifiable definition of these frequently touched surfaces based on observations assessing the frequency of healthcare worker contact with surfaces in a patient’s immediate environment. During an 18-month period in 2008–2009, the researchers observed healthcare workers (including registered nurses, physicians, nursing aides, and other allied direct-care providers) providing routine patient care, to ascertain the frequency of contact with surfaces in the immediate vicinity of the patient. A total of 50 interactions were observed in five intensive care units (ICUs) and on seven general medical-surgical floors at a 780-bed, tertiary care academic facility.
A total of 1,490 surface contacts were recorded during the observation period; the ICUs accounted for 1,109 (74 percent) surface contacts, and the medical-surgical floors accounted for 381 (25 percent). Three surfaces (the bed rail, the bed surface, and the supply cart) in the ICUs that were considered high-touch surfaces (defined as sustaining more than three contacts per interaction), and these surfaces accounted for 40 percent of the contacts recorded in the ICUs. Four surfaces (the bed rail, the over-bed table, the intravenous pump, and the bed surface) on the medical-surgical floors that were considered high-touch surfaces (defined as sustaining more than one contact per interaction, and these surfaces accounted for 48 percent of the contacts recorded on the medical-surgical floors. According to the researchers, bed rails had the highest frequency of contact in both types of healthcare settings, accounting for 7.76 contacts per interaction in the ICUs and 3.12 contacts per interaction on the medical-surgical floors.

Huslage, et al. (2010) report that for the remaining surfaces observed in the ICUs, 11 surfaces that were considered medium-touch surfaces (a mean of 1.75 contacts per interaction) and 14 surfaces that were considered low-touch surfaces (a mean of 0.52 contacts per interaction. For the remaining surfaces observed on the medical-surgical floors, seven surfaces were considered medium-touch surfaces (a mean of 0.74 contacts per interaction) and 13 surfaces that were considered low-touch surfaces (a mean of 0.20 contacts per Interaction).

It has been established by numerous studies that contaminated surfaces in patient rooms have been linked to patient-to-patient transmission of several important nosocomial pathogens, and further studies have indicated that patients admitted to rooms previously occupied by individuals infected or colonized with MRSA, VRE or C. difficile are at significantly higher risk of acquiring these organisms from contaminated environmental surfaces. The challenge is that environmental cleaning continues to be suboptimal in many facilities; studies have identified significant opportunities in hospitals to improve the cleaning of frequently touched objects in the patient’s immediate environment. Studies conducted by Carling (2006 and 2008) show that of 20,646 standardized environmental surfaces (14 types of objects), only 9,910 (47.9 percent) were cleaned during terminal room cleaning.

As Huslage, et al. (2010) observe, "Our data demonstrated that, in the ICU and on the medical-surgical floor, high-touch and medium-touch surfaces were in the immediate vicinity of the patient. This finding becomes a primary concern when considering how to target room disinfection practices. Ideally, all surfaces should be disinfected regardless of the frequency of contact, but fewer than 50 percent of surfaces are cleaned during a terminal cleaning. Hospital protocols for room cleaning and disinfection should focus on environmental service personnel training, use of checklists, and/or monitoring of those surfaces that have the highest frequency of contact with healthcare workers’ hands, to minimize the potential for hand contamination, as well as direct transmission to patients. Thus, in the ICU, it is critical that bed rails, bed surfaces, and supply carts be adequately cleaned and disinfected. Furthermore, studies of the effectiveness of room disinfection should focus on evaluating disinfection of these surfaces. Room decontamination protocols used in hospitals should take into account both our data on the frequency with which healthcare workers touch certain surfaces and data on the concentration and type of microbial pathogens found on specific environmental surfaces. Although it is desirable that all environmental surfaces be routinely disinfected, other surfaces that are likely not heavily contaminated or frequently touched, such as thermostats, may not warrant as much concern. However, at terminal cleaning, all environmental surfaces should be disinfected."
Hand hygiene is part of a multi-model approach to infection prevention and control, and must be seen as a critical intervention just as environmental cleaning is. And just like surface cleaning, hand hygiene compliance is also suboptimal; studies report compliance rates less than 50 percent in the United States, according to a review of the literature by Erasmus, et al. (2010). In the intensive care unit, studies indicate a median compliance rate in the range of 40 percent to 50 percent. Also according to Erasmus, et al. (2010), studies showed lower compliance among physicians than among nurses. Numerous studies point to similar findings. Kingston, et al. (2016) conducted a systematic study on hand hygiene compliance and suggested that the very best hand hygiene compliance achievable is around 57 percent following a period of infection control interventions, with an average of 34 percent at other times.

Some in the medical community struggle with the correlation between hand hygiene and its impact on infection rates, citing a lack of definitive studies documenting this connection. As WHO (2009) states, "The lack of scientific information on the definitive impact of improved hand hygiene compliance on HAI rates has been reported as a possible barrier to appropriate adherence with hand hygiene recommendations. However, there is convincing evidence that improved hand hygiene through multimodal implementation strategies can reduce infection rates. In addition, although not reporting infection rates, several studies showed a sustained decrease of the incidence of multidrug-resistant bacterial isolates and patient colonization following the implementation of hand hygiene improvement strategies. Failure to perform appropriate hand hygiene is considered the leading cause of HAI and spread of multidrug-resistant organisms, and has been recognized as a significant contributor to outbreaks."

We must remember that hand hygiene can at least address some of the mitigating factors involved in hand carriage of infectious agents and its role in breaking the chain of infection. For example, we know that organisms are present on patient skin and in the inanimate environment, and that healthcare-associated pathogens can be recovered from frequently colonized areas of normal, intact patient skin as well as any surgical wounds or other clinical conditions.

As Bolon (2016) reminds us, "Two classifications of skin flora have been delineated: transient flora and resident flora. Transient flora are those associated most frequently with healthcare-associated infections and are, therefore, the primary target of hand hygiene within the health care setting. Transient flora reside in the uppermost level of the stratum corneum and are acquired by direct contact with patients or with environmental surfaces associated with patients. These loosely adherent organisms can be transmitted to other patients or to the environment if they are not removed by mechanical friction, the detergent properties of soap and water, or killed by antiseptic agents. Numerous pathogens have been identified among the transient flora of healthcare workers’ hands, including S aureus, Klebsiella pneumoniae, Acinetobacter spp., Enterobacter spp., and Candida spp. Healthcare workers with skin damage or chronic skin conditions are more likely to be colonized with pathogenic organisms in greater quantities (both the number of different organisms and the bacterial counts), which can make them more likely to transmit infectious pathogens. Resident flora are the low-pathogenicity, permanent residents of the deeper layers of the skin. These organisms cause infection only when a normal barrier is disrupted, such as with the placement of an intravenous catheter. Resident flora cannot be removed solely by mechanical friction; thus, an antiseptic agent must be used before the performance of invasive procedures."

And as WHO (2009) states, "Because nearly 106 skin squames containing viable microorganisms are shed daily from normal skin, it is not surprising that patient gowns, bed linen, bedside furniture and other objects in the immediate environment of the patient become contaminated with patient flora, and numerous studies have indicated the persistence of bacteria and viruses. Patient-care activities can result in transmission of patient flora to healthcare workers' hands; in one study, Pittet and colleagues studied contamination of healthcare personnel’ hands before and after direct patient contact, wound care, intravascular catheter care, respiratory tract care or handling patient secretions. Using agar fingertip impression plates, they found that the number of bacteria recovered from fingertips ranged from 0 to 300 colony-forming units (CFUs). Studies have shown that the use of gloves did not fully protect healthcare worker’ hands from bacterial contamination, and glove contamination was almost as high as ungloved hand contamination following patient contact. Studies also indicate that organisms are frequently transferred to the hands of healthcare workers who touched both the skin of patients and surrounding environmental surfaces. Laboratory-based studies have shown that touching contaminated surfaces can transfer some organisms to the fingers. More studies are needed to determine if healthcare personnel hand contamination resulted in the transmission of pathogens to susceptible patients.

As WHO (2009) summarizes, "… contaminated hands could be vehicles for the spread of certain viruses and bacteria. Healthcare workers’ hands become progressively colonized with commensal flora as well as with potential pathogens during patient care. Bacterial contamination increases linearly over time. In the absence of hand hygiene action, the longer the duration of care, the higher the degree of hand contamination. Whether care is provided to adults or neonates, both the duration and the type of patient care affect healthcare workers’ hand contamination. The dynamics of hand contamination are similar on gloved versus ungloved hands; gloves reduce hand contamination, but do not fully protect from acquisition of bacteria during patient care. Therefore, the glove surface is contaminated, making cross-transmission through contaminated gloved hands likely."

What's more, inadequate hand cleansing, resulting in hands remaining contaminated. As WHO (2009) emphasizes, "Obviously, when healthcare workers fail to clean their hands between patient contact or during the sequence of patient care – in particular when hands move from a microbiologically contaminated body site to a cleaner site in the same patient – microbial transfer is likely to occur. To avoid prolonged hand contamination, it is not only important to perform hand hygiene when indicated, but also to use the appropriate technique and an adequate quantity of the product to cover all skin surfaces for the recommended length of time."

To interrupt transmission of HAIs spread via healthcare workers’ hands, it is useful to consider the sequence of events necessary for this to occur:
1. Organisms present on the patient’s skin or in the proximity of the patient are transferred to the hands of the healthcare worker
2. Organisms must be capable of surviving for a short period on the hands of the healthcare worker
3. Hand hygiene is inadequate, performed with an inappropriate agent, or omitted entirely
4. Contaminated hands of the healthcare worker must come in direct contact with another patient or with an inanimate object that will come in direct contact with the patient.

As Bolon (2016) emphasizes, "The contribution of contact with the immediate patient environment (as opposed to the patient directly) to the contamination of healthcare workers’ hands must be emphasized. Viable organisms are present in the 106 skin squames that humans shed daily; these may proceed to contaminate patient gowns, bed linen, and furniture. Organisms that are resistant to desiccation, such as staphylococci and enterococci, may thereby join transient flora on the hands of healthcare workers."

The World Health Organization (WHO) confirms that transmission of healthcare-associated pathogens occurs from one patient to another via healthcare workers’ hands, and also makes a case for the importance of the environment. WHO (2013) explains that, "Contamination of the inanimate environment has also been detected on ward handwash station surfaces and many of the organisms isolated were staphylococci. Tap/faucet handles were more likely to be contaminated and to be in excess of benchmark values than other parts of the station. This study emphasizes the potential importance of environmental contamination on microbial cross-contamination and pathogen spread. Certain Gram-negative rods, such as Acinetobacter baumannii, can also play an important role in environmental contamination due to their long-time survival capacities."

Organism transfer to healthcare workers’ hands is key, and as WHO (2013) points out, "Relatively few data are available regarding the types of patient-care activities that result in transmission of patient flora to HCWs’ hands. In the past, attempts have been made to stratify patient-care activities into those most likely to cause hand contamination, but such stratification schemes were never validated by quantifying the level of bacterial contamination that occurred … Pittet and colleagues studied contamination of HCWs’ hands before and after direct patient contact, wound care, intravascular catheter care, respiratory tract care or handling patient secretions. Using agar fingertip impression plates, they found that the number of bacteria recovered from fingertips ranged from 0 to 300 CFU. Direct patient contact and respiratory tract care were most likely to contaminate the fingers of caregivers. Gram-negative bacilli accounted for 15 percent of isolates and S. aureus for 11 percent. Importantly, duration of patient-care activity was strongly associated with the intensity of bacterial contamination of HCWs’ hands in this study."

Several other studies have documented that HCWs can contaminate their hands or gloves with Gram-negative bacilli, S. aureus, enterococci or C. difficile by performing “clean procedures” or touching intact areas of skin of hospitalized patients (WHO, 2013). One study that involved culturing HCWs’ hands after various activities showed that hands were contaminated following patient contact and after contact with body fluids or waste, while another study involving HCWs caring for patients with VRE, 70 percent of HCWs contaminated their hands or gloves by touching the patient and the patient’s environment. Bhalla and colleagues studied patients with skin colonization by S. aureus (including MRSA) and found that the organism was frequently transferred to the hands of HCWs who touched both the skin of patients and surrounding environmental surfaces. Hayden and colleagues found that HCWs seldom enter patient rooms without touching the environment, and that 52 percent of HCWs whose hands were free of VRE upon entering rooms contaminated their hands or gloves with VRE after touching the environment without touching the patient. Additionally, laboratory-based studies have shown that touching contaminated surfaces can transfer S. aureus or Gram-negative bacilli to the fingers.

WHO (2013) says that studies "demonstrate that contaminated hands could be vehicles for the spread of certain viruses and bacteria. HCWs’ hands become progressively colonized with commensal flora as well as with potential pathogens during patient care. Bacterial contamination increases linearly over time. In the absence of hand hygiene action, the longer the duration of care, the higher the degree of hand contamination. The dynamics of hand contamination are similar on gloved versus ungloved hands; gloves reduce hand contamination, but do not fully protect from acquisition of bacteria during patient care. Therefore, the glove surface is contaminated, making cross-transmission through contaminated gloved hands likely." WHO (2013) adds, "Obviously, when HCWs fail to clean their hands between patient contact or during the sequence of patient care – in particular when hands move from a microbiologically contaminated body site to a cleaner site in the same patient – microbial transfer is likely to occur. To avoid prolonged hand contamination, it is not only important to perform hand hygiene when indicated, but also to use the appropriate technique and an adequate quantity of the product to cover all skin surfaces for the recommended length of time."

As we have seen, cross-transmission of organisms occurs through contaminated hands. Factors that influence the transfer of microorganisms from surface to surface and affect cross-contamination rates are type of organism, source and destination surfaces, moisture level, and size of inoculum. Harrison and colleagues showed that contaminated hands could contaminate a clean paper towel dispenser and vice versa. The transfer rates ranged from 0.01 percent to 0.64 percent and 12.4 percent to 13.1 percent, respectively. A study by Barker and colleagues showed that fingers contaminated with norovirus could sequentially transfer virus to up to seven clean surfaces, and from contaminated cleaning cloths to clean hands and surfaces.

The chain of transmission teaches us that clean hands that touch contaminated surfaces can transmit pathogens; inversely, dirty hands that touch clean surfaces can also serve as a method of transferring microorganisms. Pulling this concept together is research showing that hands are contaminated about equally after contact with patient skin and surfaces. Stiefel, et al. (2007) demonstrated that hand contamination was likely to be equal after contact with commonly examined patient skin sites and commonly touched environmental surfaces in patient rooms, and that their findings suggest that contaminated surfaces may be an important source of methicillin-resistant Staphylococcus aureus (MRSA) transmission. 

As the researchers note, "The relative importance of environmental surfaces compared with patients’ skin as a source for contamination of the hands of healthcare workers is unclear. Because some studies suggest that acquisition of S. aureus on hands is common after contact with contaminated surfaces, we hypothesized that the frequency of MRSA acquisition and the quantity of MRSA acquired on hands is similar after contact with skin sites and environmental surfaces in the rooms of MRSA carriers."

In their two-month study at a 285-bed Veterans Affairs hospital that conducts surveillance for anterior nares carriage of MRSA for all inpatients, the researchers enrolled a sample consisting of 40 patients admitted with MRSA colonization or infection. During the study, sodium hypochlorite (5,000 ppm) was used for disinfection of rooms after discharge of MRSA patients, but high-touch surfaces were not cleaned on a daily basis unless they were visibly soiled. The researchers obtained samples for gloved hand-imprint cultures from patient skin sites such as the abdomen, chest, forearm, and hand, as well as from environmental sites including the bed rail, bedside table, telephone, and call button, to compare the risk of hand contamination after contact with skin compared with the environment,

Stiefel, et al. report that the risk of any gloved-hand contamination after contact with the skin sites and the environmental surfaces was not significantly different (40 percent versus 45 percent). They add that there was also no significant difference in the mean number of colony-forming units (CFUs) per gloved handprint acquired after contact with skin and environmental sites. The most frequent skin and environmental sites associated with hand acquisition were the abdomen or chest and the call button, respectively. Of the skin sites, patients’ abdomen had the highest number of colonies acquired on gloved hands. Of the environmental sites, the call button had the highest number of colonies acquired by gloved hands.

The researchers write, "Our findings have several practical implications for control of MRSA. First, our findings provide support for the recommendation that healthcare workers routinely disinfect their hands after contact with inanimate objects in the immediate vicinity of patients. In our facility, healthcare workers’ compliance with hand hygiene is statistically significantly lower after contact with environmental surfaces only compared with that after contact with patients (authors’ unpublished data), suggesting that healthcare workers need education regarding the importance of the environment as a source for hand contamination. Second, because MRSA may survive for long periods on surfaces, our findings reinforce the importance of environmental disinfection after discharge of MRSA patients. Finally, it is possible that daily disinfection of high-touch surfaces in MRSA isolation rooms might reduce the level of contamination and decrease the risk for acquisition on healthcare workers’ hands."

More recently, Barnes, et al. (2014) developed an agent-based model of patient-to-patient transmission-via the hands of transiently colonized healthcare workers and incompletely terminally cleaned rooms-in a 20-patient intensive care unit. Nurses and physicians were modeled and had distinct hand hygiene compliance levels on entry and exit to patient rooms. The researchers simulated the transmission of Acinetobacter baumannii, methicillin-resistant Staphylococcus aureus, and vancomycin-resistant enterococci for one year using data from the literature and observed data to inform model input parameters.

The researchers simulated 175 parameter-based scenarios and compared the effects of hand hygiene and environmental cleaning on rates of multidrug-resistant organism acquisition. They reported that for all organisms, increases in hand hygiene compliance outperformed equal increases in thoroughness of terminal cleaning. From baseline, a 2:1 improvement in terminal cleaning compared with hand hygiene was required to match an equal reduction in acquisition rates (e.g., a 20 percent improvement in terminal cleaning was required to match the reduction in acquisition due to a 10 percent improvement in hand hygiene compliance). Barnes, et al. (2014) emphasize that hand hygiene should remain a priority for infection control programs, but environmental cleaning can have significant benefit for hospitals or individual hospital units that have either high hand hygiene compliance levels or low terminal cleaning thoroughness.

As Barnes, et a. (2014) note, "Environmental disinfection and hand hygiene are two pillars of infection prevention, however, the relative importance of each in the healthcare setting is unknown. We explored the relative impact of hand hygiene and environmental cleaning on acquisition of MDROs including MDR-A. baumannii, MRSA and VRE by using an agent-based model. According to our model, hand hygiene is a more efficient strategy for preventing transmission of MDROs and in general a 2:1 improvement in thoroughness of terminal cleaning compared to hand hygiene compliance is required to achieve an equal reduction in acquisition rates for all MDROs tested. Furthermore, strategies of solely hand hygiene improvement outperformed terminal cleaning alone or mixed strategies. The importance of hand hygiene is emphasized in the scenarios that involved an MDRO of low environmental impact, that is, those in which the risk of acquisition from the prior-room occupant is lower (e.g., MRSA, VRE, or the low-risk MDR-A. baumannii scenarios). In these situations, strategies that included hand hygiene improvements, either alone or in combination with improvements in environmental cleaning, performed significantly better than for the high-risk A. baumannii scenarios, where there was little benefit at total percent improvement levels of 30 percent or higher. This trend suggests that, for organisms with low environmental impact, some effort to improve hand hygiene compliance should accompany any strategy to improve terminal cleaning."

The researchers emphasized that it was unclear if their findings suggest favoring investment in hand hygiene compliance over improving environmental cleaning: "For each of the organisms modeled, a benefit was seen for each increment of improvement in terminal cleaning, consistent with the clinical studies on which our modeling was based, that environmental hygiene has an important role in the prevention of MDRO acquisition and possible infection. This effect may be most pronounced in scenarios that include an MDRO with a significant environmental risk (e.g., the high-risk MDR-A. baumannii), which suggest that if improvements in terminal cleaning thoroughness above 30 percent can be achieved, a strategy focusing solely on environmental cleaning may be of greater benefit. The literature suggests that thoroughness of terminal cleaning is 40 percent on average and studies have shown that specific interventions may enhance cleaning to 78–88 percent. For facilities with low baseline levels of compliance of both hand hygiene and environmental cleaning, the question may then be, which strategy is easiest to employ? This is dependent on facility characteristics, personnel and whether improvements in terminal cleaning are easier to achieve than improvements in hand hygiene compliance. If terminal cleaning is more easily improved (as may be the case in many settings), then improving thoroughness may be the more effective strategy."

Making a strong case for environmental cleaning were Otter, et al. (2013), who say that, "Evidence that contaminated surfaces contribute to the transmission of hospital pathogens comes from studies modeling transmission routes, microbiologic studies, observational epidemiologic studies, intervention studies, and outbreak reports." They add, "In vitro studies of the spread of DNA or other markers, model organisms, or pathogens show that transfer can occur from environmental surfaces to hands and vice versa. Several microbiologic studies have investigated the transfer of pathogens from surfaces to the hands or gloves of healthcare personnel in the absence of direct patient contact. Contact with an environmental surface carries approximately the same risk of acquiring MRSA, VRE and C difficile hand or glove contamination as touching an infected or colonized patient. One study estimated that VRE hand contamination was acquired through approximately 10 percent of contacts with either the patient or the surfaces surrounding the patient. Importantly, hand hygiene compliance was significantly more likely following direct patient contact compared with contact with the patient environment, meaning that contamination acquired from the environment is likely to persist for longer and hence could be relatively more important for onward transmission."

Otter, et al. (2013) explain that strategies to address environmental contamination can be divided into reducing and containing the shedding of pathogens and improved cleaning and disinfection: "Improving compliance with hand hygiene following contact with a patient’s surroundings will reduce the chances of indirect spread of pathogens acquired on the hands of healthcare personnel following contact with their surroundings. Also, improved compliance with hand hygiene before and after direct contact with patients will reduce the spread of contamination into the healthcare environment on the hands of healthcare personnel." Regarding cleaning and disinfection, Otter, et al. (2013) note, "Effective cleaning and disinfection relies on the operator to repeatedly ensure adequate selection, formulation, distribution, and contact time of the agents used. Educational improvements designed to modify human behavior can be attempted with the support of various tools including fluorescent markers or adenosine triphosphate assays, and monitoring and feedback can improve the frequency of surface cleaning, reduce the level of environmental contamination, and reduce the acquisition of pathogens. However, no studies have evaluated the sustainability of such systematic improvements. Indeed, recent evidence indicates that altering the location of florescent dye spots reduced the proportion of objects that were cleaned from 90 percent to approximately 60 percent. Improvements in hospital design and materials, novel disinfectants, and cleaning/disinfection technologies should be evaluated to determine their effectiveness in improving cleaning and disinfection. For example, there has been recent discussion on 'no-touch' automated room disinfection (NTD) systems, which remove or reduce the reliance on the operator to achieve adequate distribution and contact time of the active agents. HPV, aerosolized hydrogen peroxide, ultraviolet C, and pulsed-xenon ultraviolet radiation NTD systems have all shown promise and improved efficacy when compared with conventional methods. NTD systems are only appropriate for certain applications and should be introduced in parallel with an educational campaign to improve conventional methods. Antimicrobial or “self-disinfecting” surfaces and air disinfection units have shown some promise in reducing the environmental bioburden, but further evaluations with clinical outcomes are required. The most appropriate strategies to address surface contamination will depend on the setting and on local epidemiology."

Donskey (2013) examined the evidence that improving environmental disinfection can reduce HAIs and outlined four sources of transmission and potential environmental disinfection strategies to interrupt transmission:
1. Contamination of surfaces after terminal cleaning of isolation rooms resulting in risk of acquisition by patients subsequently admitted to the same room (intervention: improve terminal room cleaning and disinfection)
2. Contamination of surfaces in isolation rooms resulting in risk for contamination of health care personnel hands (intervention: daily disinfection of high-touch surfaces)
3. Contamination of portable equipment (intervention: disinfection of portable equipment between patients or use of disposable equipment in isolation rooms)
4. Contamination of surfaces in rooms of unidentified carriers of healthcare-associated pathogens (intervention: improve cleaning and disinfection of all rooms on high-risk wards or throughout a facility).

Based on these routes of transmission, Donskey (2013) highlighted four potential environmental disinfection strategies to reduce transmission:
- First, improving cleaning and disinfection of rooms of patients known to carry healthcare-associated pathogens after discharge (i.e., terminal cleaning) will reduce the risk that patients subsequently admitted to the same room will acquire pathogens from contaminated surfaces.
- Second, daily disinfection of high-touch surfaces in isolation rooms may be useful to reduce the risk of contamination of the hands of healthcare personnel providing care for the patients. This strategy is analogous to daily disinfection of the skin of patients as a means of source control to reduce transmission of MRSA and VRE.
- Third, disinfection of portable equipment between patients or use of disposable equipment in isolation rooms will reduce the risk for transmission.
- Finally, rather than focusing only on isolation rooms, efforts to improve cleaning and disinfection of all rooms may be beneficial if there is a concern that many carriers are not identified or are identified only after long delays.

Tackling the issue of an integrated approach to hand hygiene and environmental cleaning is Philip Carling, MD, Carling, director of infectious diseases and hospital epidemiology at Carney Hospital in Boston, as well as professor of clinical medicine at Boston University School of Medicine. Carling, who has conducted numerous studies addressing the need for proper and robust environmental hygiene in hospitals, says that to move the needle on cleanliness overall, hand hygiene and environmental cleaning must be integrated and multi-modal. He says this imperative is so challenging for facilities because "it has not been on their radar screens," and adds, "The issue has not been recognized by the hand hygiene leaders, and the Joint Commission is all about antimicrobial stewardship and they do not deal well with multiple priorities."

As Carling (2016) observes, "Over the past several years, it has become increasingly evident that infection prevention initiatives focused on optimizing hand hygiene have not realized their hoped-for impact on HAP transmission in well-resourced healthcare settings. Accepting an inability to quantify the absolute risk of pathogen acquisition directly from healthcare workers’ hands, there is good circumstantial evidence that such transmission accounts for a substantial proportion of HAP transmission. It has become widely accepted that hand hygiene, as noted by Palamore and Henderson, is 'critically important for the prevention of HAIs.'  In response, many healthcare organizations have undertaken extensive, resource-intensive efforts to improve hand hygiene compliance.  Despite extensive translational research and strong support from accrediting institutions over the past 10 years, the enthusiasm for quickly reaping substantial benefits from optimizing hand hygiene practice has been tempered by the realization that acceptance inertia, psychological barriers, suboptimal application of technique, and, most particularly, the pressures of providing direct patient care have had an adverse impact on the effectiveness of this intervention. These issues, along with the challenges of performing hand hygiene as recommended by the World Health Organization 'five moments' construct while caring for acutely ill patients and the fact that 10 percent to 60 percent of patient zone surfaces contain HAPs, make it likely that pathogen-contaminated environmental surfaces will negate some of the benefits of optimized hand hygiene practice."

Carling (2016) offers a schematic that seems to indicate a possible path toward improvement: "Given that patient zone surfaces not contaminated by HAPs cannot be a source of pathogen transmission even in the absence of hand hygiene, further consideration must be given to viewing both environmental hygiene and hand hygiene as interdependent interventions. When viewed in this manner, it becomes evident that the mandates and challenges of these two interventions represent an inverse continuum. For example, in the ICU setting, where hand hygiene often becomes logistically challenging and glove use without hand hygiene is frequent, there would be a particularly strong mandate to optimize hygienic cleaning. In contrast, in ambulatory settings, where there are few intrinsic barriers to hand hygiene, enhanced hygienic cleaning practices would not be strongly mandated. In this context, the specific elements of hygienic practice can be characterized along a complexity gradient. By relating these constructs to the various settings, interventions can be defined along the continuum outlined to provide a framework for analyzing and prioritizing the relative cost/benefit of different levels of complementary hygienic practices. By characterizing intrinsic patient/personnel risk and setting modifiers, a particular site can be moved up or down diagonally along the range of settings. For example, if an immunologically compromised person was in an ambulatory care setting it would be reasonable to consider moving to a higher level of hygienic cleaning intervention than otherwise is warranted. Similarly, if the patient population in a long-term care setting required only minimal assistance, it would be reasonable to move down the intervention continuum toward noninpatient healthcare settings. Once the particular features of a setting are defined in this manner, the constructs can be used to develop programmatic interventions that maximize the components of healthcare hygienic practice for the best cost/benefit to improving patient/personnel safety."

Carling (2016) points to a lack of guidance and emphasizes the need for consensus-based research agenda that can address the current state of knowledge regarding how patient-care surfaces become contaminated, how transmission of infections occurs from the surfaces, and what facilities can do to improve the cleanliness of these surfaces. Additional research should help define the quantitative impact of hand hygiene and environmental cleaning, and it is critical that all stakeholders, including industry, come together to address unresolved issues. Regarding the hope that researchers and industry can collaborate to better provide actionable evidence that end-users in hospitals can put into practice, Carling says, "There is a tiny bit of movement but it is not flashy, and it takes committed leadership and some carrot or stick to get people to wake up.  Most of the HAI prevention-related industries find it much better to spend money on marketing and almost nothing on research, especially translational research. Actionable evidence is out there, as noted in my review, but only a few healthcare epidemiologists and infection preventionists are interested."

As Carling (2016) observes, "…it is hoped that the rapidly evolving technology, including the use of genomic epidemiology tools, highly sensitive and standardized surface culture methods, and sensitive approaches to pathogen acquisition monitoring will begin to clarify ways to optimize these interventions."

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