By Kelly M. Pyrek

This article originally appeared in the January 2020 issue of Healthcare Hygiene magazine.

Fomites flying under the radar is common in the fast-paced, demanding healthcare environment and constitute a challenge for the professionals who are tasked with cleaning and disinfecting them.

“Each institution and sometimes each unit has a different way of cleaning things,” acknowledges Mark E. Rupp, MD, professor and chief of the Division of Infectious Diseases, and medical director of the Department of Infection Control & Epidemiology at the University of Nebraska Medical Center. “Oftentimes it takes someone going in and taking inventory of objects in the room and establishing who is cleaning what.”

Rupp adds, “Point-of-care ultrasound is our current project.  However, there are lots of items – all the things that are touched frequently are worrisome – keyboards, phones, everything near the patient – switches, buttons, handles, etc.  Stethoscopes are another item that healthcare workers carry around and rarely clean between patients.  In many instances, anything that is electronic is not cleaned by environmental services (EVS) – the patient-care staff think that EVS is cleaning screens and monitors and pumps, etc.  EVS workers are concerned that they will damage the equipment, or, for daily clean, that they will set off an alarm or turn off a pump, etc.  Thus, in too many instances, no one is cleaning the items because people want to believe that someone else is doing the cleaning.” (See related article on page 16 of this issue.)

As we know, a fomite, defined as "an inanimate object that can be the vehicle for transmission of an infectious agent," includes patient-care items and environmental surfaces.  Kanamori, et al. (2017) remind us that, “It has been demonstrated that such items (e.g., medical equipment, surfaces) are frequently contaminated and can serve as a reservoir or source for multidrug-resistant organisms (MDROs) such as methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), and Clostridium difficile. Transmission of MDROs from contaminated devices or surfaces to a patient may occur via direct contact, indirectly via the hands/gloves of healthcare personnel, or less commonly via aerosols, water, or food.”

How fomites become contaminated and contribute to transmission dynamics is a key factor in improving environmental hygiene in healthcare institutions. To this end, Xiao, et al. (2019) developed a model to simulate the dynamic transmission of MRSA among fomites in a general medical ward, as well as conducted network analyses to better understand the contact relationship between patients’ hands and environmental surfaces. They also investigated the effectiveness of applying different levels of two interventions to seven types of surfaces and utilized the MRSA distribution patterns and network analyses to account for the findings. They report that frequent surface cleaning and antimicrobial surfaces had larger impacts on MRSA exposures when applied to surfaces around the index and the adjacent patients and to public surfaces in the ward than when applied to surfaces around other susceptible patients in the ward.

Specifically, to better understand how different surfaces work in fomite-related transmission, the researchers modeled the structure of the relationships between human hands and environmental surfaces as a network; they explain that, “The multiple environmental surfaces in indoor environments are not independent but are linked by hands through human touching behaviors, thus constructing a surface touch network. In this network, a node denotes a surface, and an edge means a contact between the two connected surfaces. Since the healthcare worker’ (HCW)’s routine round behaviors only occurred at special time points, the HCW’s hand are not included in the network analysis. To analyze the surface touch network, we calculated the distances between surfaces and centrality measures (including the degree, betweenness and closeness centralities) of surfaces. The distance, defined as the number of edges in the shortest path connecting two surfaces, indicates how fast contaminants diffuse across multiple surfaces.”

The researchers tested two intervention methods on bedding surfaces, bedside table surfaces, as well as public surfaces in the ward, and assumed a baseline scenario where surface cleaning was not performed. They hypothesized several improved scenarios for the two intervention methods: with 1,000 ppm sodium hypochlorite, surface cleaning could yield a 0.70 to 1.65 log10 reduction of MRSA on surfaces; with the use of inefficacious disinfectants or incorrect surface cleaning methods, the reduction could be low, such as 25 percent.

The researchers found that, with enough touching behaviors, the MRSA concentration on surfaces presented a stable daily cycle, due to a balance between the MRSA generation and removal mechanisms (including hand hygiene and MRSA inactivation on surfaces). They say the difference in surface touching frequencies at night and in the daytime makes the MRSA concentration vary with time rather than maintain an equilibrium.

“The source bedding surfaces exhibited a different MRSA concentration pattern,” the researchers report. “Since the transfer rate from hands to porous surfaces was much larger than that from porous surfaces to hands, MRSA concentration on the source bedding surface followed the frequency of touching behaviors and was quite high in the daytime and decreased at night. Further, at night, the gain of MRSA to bedding surfaces was lower than the inactivation, so the MRSA concentrations on the source bedding surfaces decreased … we can infer that the optimal cleaning time for the source bedside table surfaces and hands and skins was the end of the night, while that for other surfaces was the beginning of the night.”

They continue, “Comparing different surfaces of the same patient, we found that the MRSA concentrations on bedding surfaces were always the highest, which could be explained by three reasons. First, the transfer rate of MRSA from hands to porous surfaces (0.8) was much higher than that from porous surfaces to hands, which led to a net gain of MRSA at most cases on porous surfaces during the contact. Second, the bedding surfaces were touched at a higher frequency (6/hour in the daytime and 3/hour at night) than bedside table surfaces (2/hour in the daytime and 0/hour at night), which means the net transmission from hands to bedding surfaces occurred relatively frequently. Third, the MRSA inactivation rate on the porous surfaces (0.0379/hour) is low relative to that on the skin (0.2112/hour), so MRSA could survive for a longer period on the bedding surfaces.”

Comparing surfaces of different patients, Xiao, et al. (2019) found that those of the index and the adjacent patients had much higher MRSA concentrations than those of normal patients: “Since surfaces of the index patients are sources, the MRSA concentrations on them must be higher than other surfaces to maintain a concentration gradient for the MRSA diffusion. The high MRSA concentration on surfaces of the adjacent patients was caused by HCWs’ routine rounds. During the routine rounds, HCWs directly contacted patients in a fixed sequence. After visiting the index patient, the HCW’s hands carried MRSA, of a high concentration but a limited amount due to the small area of hands. Then, most of the MRSA on the HCW’s hands were transmitted to the surfaces of the adjacent patient and led to more MRSA of the surfaces of the adjacent patient than on surfaces of normal patients.” The researchers conclude that although the MRSA concentrations on different groups of surfaces varied with the transfer rates, inactivation rates and touching frequencies, surfaces of the source patient always had the highest MRSA concentration while those of the normal patients are the lowest.

Not surprisingly, the researcher found that public surfaces had higher MRSA concentrations than surfaces of the normal patients, which might be explained by the distance of the surface touch network, in that the distance from the source to surfaces around the normal patients was 2 (hands) or 3 (bedding, bedside table and exposed skin surfaces), while the distance from the source to the public surfaces was 1. They explain, “This is consistent with graph theory, in that surfaces separated by longer distances have less communication, and thus less transport of MRSA.”

They also found that public surfaces were very influential in the entire transmission process, and that the disruption of these key surfaces had a greater impact on the topology of the network than others, indicating that intervention methods on the public surfaces could be more effective than interventions on other surfaces. Public surfaces also lay on all the paths between the surfaces of the index patient and those of others in the network. As the researchers note, “Without these public surfaces, it would be very difficult for MRSA to spread from the index patient to other patients via the fomite route. With respect to closeness centralities, the public surfaces had the highest values. The average distances from the public surfaces to any other surface were short, indicating that public surfaces are highly efficient at spreading MRSA to other surfaces.”

In the baseline scenario, the average exposure to the susceptible patients was 17.5 CFU. The researchers found that, even with a low cleaning efficacy of 0.25, the average reduction was about 0.60, which indicated surface cleaning could effectively lower the exposure. As the surface cleaning efficacy (0.25, 0.5, 0.75 and 1) increased, the corresponding average reduction (0.60, 0.69, 0.73 and 0.75) also rose, but the growth rate decreased. The researchers say that for hospitals on a limited budget, the efficacy of 0.5 is an acceptable choice, with a relatively high average reduction.

The observe, “Ideally, if we cleaned all the environmental surfaces infinite times with a cleaning efficacy of 1, these surfaces would be always clean and would not play any role in spreading the MRSA. However, since MRSA can be transmitted via HCWs’ hands, the exposure to the susceptible patients remains. Given infinite cleaning, exposure will be reduced by 0.91, which is just a little bit better than the exposure reduction achieved with a cleaning frequency of 16/day, 0.86. Thus, excess enhanced surface cleaning does not offer substantial benefits, particularly given the high financial burden of hospitals and the heavy workload of cleaners, which might inversely lead to an increased infection risk.”

To increase the efficiency of frequent cleaning, Xiao, et al. (2019) also investigated which cleaning strategies produced a high reduction of exposure to the susceptible patients.  They found that frequent cleaning on the normal patients’, the adjacent patient’s and the index patient’s surfaces had weak, modest, and strong effect on the reducing the MRSA exposure among susceptible patients, respectively: “The exposure reduction is driven by the diversity of MRSA concentrations on surfaces, as cleaning environmental surfaces with higher MRSA concentrations, such as the index patient’s surfaces, removes more MRSA, and this cascades through the network to reduce MRSA on the surfaces of susceptible patients. Many recommendations have been proposed to clean near-patient sites in hospitals, which could be made more specific. Among all the near-patient sites, more attention should be paid to effectively cleaning surfaces around the adjacent and the index patients than to cleaning surfaces around normal patients. Early detection and isolation of index patients could help prevent transmission of MRSA.”

Of note, the researchers say that for public surfaces, the association between high exposure reduction and cleaning frequency indicates that it is effective to clean these surfaces frequently: “Several studies have recommended that public surfaces such as doorknobs and surfaces in and around toilets in patients’ rooms be cleaned and disinfected on a more frequent schedule. Public surfaces are a kind of high-touch surfaces since they are touched by many people, despite the low average touching frequency by each person. They are different from another kind of high-touch surfaces around patients, such as bedding, that are touched frequently by few people. The reason that enhanced cleaning on public surfaces reduced exposure was more related to their influential role in the entire MRSA transmission process than to the frequency people touched the surfaces. Therefore, the recommendations to clean high-touch surfaces could be more specific as enhancing cleaning on public surfaces touched by many people.”

In their study, Xiao, et al. (2019) asserted that “Implementation of improved cleaning and antimicrobial surfaces on all environmental surfaces equally will be a heavy burden on healthcare resources. More efficient implementation should distinguish ‘important’ environmental surfaces that contribute significantly to infection risk in a hospital ward from others and concentrate the available cleaning resources and antimicrobial surfaces and coatings on them.”

Patient-care items are among the most frequently touched items in the healthcare environment and warrant attention. As such, Kanamori, et al. (2017) examined the role that patient-care items play in healthcare-associated outbreaks, updating their 1987 review. They note, “Fomites recognized in the previous review (humidifier, nebulizer, urine-measuring device, stethoscope, thermometer, suction apparatus, pressure transducer) have continued to be implicated in healthcare-associated outbreaks. There were also various contaminated fomites implicated without having clear evidence of healthcare-associated outbreaks and infections. During the three decades since our last review, additional healthcare fomites (hand soap/sanitizer dispenser, ultrasound probe/gel, computer keyboards) have been identified. The type of patient care items as a fomite has changed over time, and some of them were likely to be reduced nebulizer, pressure transducer, thermometer), but others were not. The number of healthcare-associated outbreaks via a patient care item may be affected by publication bias, depending on authors’ interest (rare organism or fomite) and findings.”

Let’s briefly review some of these culprits.

As for respiratory-care equipment, the literature contains reports of contaminated humidifiers, nebulizers and suction apparatus leading to infections caused by pathogens such as Acinetobacter baumannii, Burkholderia cepacian, Klebsiella oxytoca, Pseudomonas cepacia, MDR Pseudomonas aeruginosa, S. maltophilia, MDR A. baumannii, extended- spectrum β-lactamase (ESBL)–producing Klebsiella pneumoniae, Enterobacter aerogenes, and MRSA.

Rectal thermometers served as a fomite for outbreaks of Enterobacter cloacae, VRE, Clostridium difficile, and ESBL-producing K. pneumoniae, while contaminated ultrasound gels led to B. cepacia infection and bacteremia, S. aureus pyoderma, or Mycobacterium massiliense surgical site infection, while contamination of transesophageal echocardiography (TEE) probes was involved in outbreaks of E. cloacae, S. marcescens, and MDR P. aeruginosa.  Legionella pneumophila pneumonia cases were also associated with contaminated water to rinse TEE probes.

Outbreaks of S. marcescens, New Delhi metallo-β-lactamase (NDM)–producing E. cloacae, and P. aeruginosa were associated with contamination of refillable liquid soap or antibacterial soap dispensers, facilitating transmission of the pathogen via hands of healthcare personnel.

Healthcare-associated outbreaks via stethoscope occurred in combination with other reservoirs ( artificial nails, computer mouse, ointment, sink, other environment) and were caused by A. baumannii, ESBL-producing K. pneumoniae, K. pneumoniae bacteremia. metallo-β-lactamase (VIM)–producing carbapenem-resistant P. aeruginosa.

Outbreaks of C. difficile infection in non-isolation rooms or Chryseobacterium meningosepticum infection in neonates and pediatric patients implicated computer keyboards and other medical equipment. Contamination with multiple pathogens had been identified on computer keyboards, mobile phones, and tablets, and may be one of the most-studied class of fomites.

As Messina, et al. (2011) found, microbes recovered from keyboards had counts ranging from 6 CFU per key to 430 CFU per key. Mold was detected on 22 keyboards, ranging from a maximum of 120 CFU per key, while yeast was found on 17 keyboards up to a maximum of 420 CFU per key. Staphylococci were found on all keyboards but one at counts up to 120 CFU per key. S aureus was significantly more common on shared keyboards than on nonshared keyboards. As the researchers note, “Sources of bacterial contamination can include poor hand hygiene and droplets of saliva that inevitably fall on the keyboard during talking, sneezing, and coughing. Thus, to reduce the resident population of microbes with pathogenic potential, it is advisable to observe the general rules of hygiene and to clean keys frequently. To prevent transfer of bacteria to and from keyboards via users’ hands, thorough handwashing before and after keyboard contact is recommended. Handwashing is often considered laborious and is subject to low compliance, as demonstrated by some studies. Another strategy is to regularly disinfect equipment. Several studies have shown that good hygiene reduces keyboard contamination.”

Another reservoir is the use of smartphones in the clinical environment, highlighting the need to consider infection control policies to mitigate the potential risks associated with the increased use of these devices.

Simmonds, et al. (2019) sought to characterize the quantity and diversity of microbial contamination of hospital staff smartphones using culture-dependent and culture-independent methods; to determine the prevalence of antibiotic-resistant potential pathogens; and to compare microbial communities of hospital staff and control group phones. The researchers swabbed the smartphones of 250 hospital staff and 191 control group participants and determined the antibiotic resistance profile of Staphylococcus aureus and Enterococcus isolates was determined. Swabs were pooled into groups according to the hospital area staff worked in, and DNA was extracted.

Almost all (99.2 percent) of hospital staff smartphones were contaminated with potential pathogens, and bacterial colony forming units (CFUs) were significantly higher on hospital phones than in the control group. Methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant Enterococcus (VRE) were only detected on hospital mobile phones. Metabarcoding revealed a far greater abundance of Gram-negative contaminants, and much greater diversity, than culture-based methods. Bacillus spp. were significantly more abundant in the hospital group.

In their review, Kanamori, et al. (2017) say the main cause of healthcare-associated outbreaks was inappropriate disinfection practice for shared items: “Other reviews also noted that medical equipment used in noncritical settings rarely had cleaning protocol and may be involved in frequent transfer of pathogens compared to critical settings, suggesting the need for appropriate cleaning and disinfection protocols for patient care items commonly used in daily practice. Cleaning must precede high-level disinfection or sterilization of any reused patient care items. Thus, assuring disinfectants for noncritical medical equipment in addition to improving thoroughness of cleaning and disinfection practice is imperative in terms of infection prevention. As currently available disinfectants have both advantages and disadvantages, five components to help select optimal disinfectants in healthcare facilities—including relevant kill claims, appropriate wet-contact and kill times, safety, ease of use, and other factors (user training and support by the manufacturer, costs, and standardization)—have been discussed.”

They add, “Any patient-care items used in healthcare settings can be contaminated with a healthcare-associated pathogen and are a potential fomite, but outbreaks via these fomites can be prevented or minimized by adhering to current recommendations (manufacturers and CDC) for cleaning and disinfection/sterilization of devices and surfaces. Although the trend in healthcare-associated outbreaks via a fomite may be affected by reporting bias, sharing lessons learned from outbreaks and accumulation of practical evidence would help improve infection prevention for each fomite. It is important for healthcare personnel to recognize the increasing role of patient care items as a fomite and adhere to prevention strategies for fomite-associated outbreaks based on current guidelines and the literature. Further investigations for healthcare fomites, including causation between contamination of a pathogen with a fomite and actual healthcare-associated outbreaks, elucidation of direct and indirect transmission mechanisms via a fomite using advanced molecular typing, establishment of standard environmental sampling of medical equipment, and improvement of adherence to cleaning and disinfection practice against a fomite, are warranted.”

While fomites are ubiquitous in the healthcare environment, their omnipresence may make them more easily ignored as they fade into the background.

“Although fomite-mediated spread of pathogens has been illustrated in numerous clinically relevant instances and is a well-defined phenomenon, there are various questions that remain,” says the University of Nebraska Medical Center’s Mark E. Rupp. “All healthcare providers should be aware of this route of dissemination and means to prevent such spread.  However, as medical care has become more complex and technologically oriented, an increasing array of potential fomites have been introduced into medical care.”

As we have seen, some researchers say emphasis should be placed on high-touch, near-patient objects and surfaces only. “Potential fomites that pose the greatest risk are those that are more likely to harbor large numbers of pathogens, are difficult to clean/disinfect, come into contact with a patient’s bloodstream or mucus membranes, or are found in conjunction with particularly high risk patients,” Rupp says. “So, for example, a blood pressure cuff in an ambulatory clinic caring for largely healthy patients should be cleaned between patients with a low-level disinfectant.  However, it generally comes into contact only with a patient’s intact skin (or sometimes I’ve seen clinics where they measure blood pressure through a patient’s shirt sleeve – so in some instances it may be in contact with clothing) and, in a clinic caring for largely healthy persons, the risk is fairly low that a dangerous pathogen is going to be transferred from one person to another and result in invasive disease.  Conversely, for example, an ultrasound probe used in a NICU to establish vascular access may deliver pathogens in close proximity to the vascular system – in the presence of a foreign body (IV) - in a very vulnerable population (neonate).  It is thus imperative that the ultrasound probe and machine be appropriately cleaned between patients.”

Considering the degree of contamination of the environment by specific pathogens is a key factor when examining the role fomites play in infection transmission.

“In a perfect world, all potential fomites would be appropriately cleaned and disinfected after use and between patients or eliminated altogether,” Rupp says. “However, there are a myriad of potential fomites and, as already noted, some can pose a more serious threat than others. We don’t live in a perfect world and resources for our environmental service personnel and clinical support staff are limited.  Thus, the degree of likely contamination, what it is likely to be contaminated with, and who it is going to potentially transmit to are important considerations.   So, in the previous example of the blood pressure cuff, for the average patient in an ambulatory clinic – I won’t lose too much sleep.  The same blood pressure cuff used in a patient with fecal incontinence and widespread skin contamination who is known to be colonized with a pan-resistant Acinetobacter who is being cared for in a clinic that is specialized for solid organ transplant patients – you bet I’m concerned.

Confounders such as hand hygiene and the quality of cleaning come into play when evaluating how fomites contribute to the spread of pathogenic organisms.

“Hand hygiene is critical,” Rupp confirms. “For example, cell phones are ubiquitous and are in every healthcare worker’s pocket. They chime while a nurse or doctor cares for a patient and often they are tended to. The phone becomes contaminated and is rarely cleaned (lots of studies looking at contamination of all sorts of things – phones, beepers, neck ties, wrist watches, etc.).  It is important that after the phone is dealt with, the healthcare worker uses the alcohol gel to disinfect hands before going back to their patient.  Similarly, if the environmental services team is doing a good job in daily and terminal cleaning, the burden of contamination is decreased, making it less likely that hands or fomites become contaminated and carry pathogens to the next patient.

Improved cleaning and disinfection, after controlling for other interventions, has been found to reduce the risk of patient infection, according to studies, and Rupp says that experts can argue about the relative benefit for any intervention. “The studies that try to isolate the importance of hand hygiene, environmental cleaning, fomite elimination, etc. are difficult to do, are usually underpowered, and are often fraught with confounding,” he adds.  “However, taken together, the data clearly demonstrates that the environment becomes contaminated and can stay so for long periods of time, the environment can serve as a vehicle or reservoir for transmission to hands and clothing of healthcare personnel and sometimes directly to patients. Environmental cleaning, when done properly, effectively diminishes the amount of contamination and results in decreased transfer to hands, clothing, and patients. We can discuss all day and still not know if this results in 5% of nosocomial transmission or 50 percent (probably somewhere in between).”

Rupp continues, “When we consider cross-colonization of patients from the inanimate environment, should we be using tools such as molecular epidemiologic techniques to identify pathogens, should we be measuring the quality of environmental cleaning and hand hygiene over time, and should we think about the link between contaminated surfaces and cross-colonization events in geographic and temporal dimensions?”

Rupp adds, “Use of molecular epidemiologic tools – up to whole genomic sequencing – can be very helpful in understanding the dynamics of transmission.  These tests are often expensive and time consuming and are probably out of the question in most instances.  However, measurement, reporting, and optimization of hand hygiene compliance and environmental cleaning (including fomites) should be routinely done by all healthcare organizations. Leadership should be involved. All providers should be interested in and know their unit and organizational infection rates, cleaning effectiveness, hand hygiene compliance, etc.  If an organization is doing all this right, they don’t need to be nearly as concerned that the “superbug’ of the day is going to find a nesting spot in their facility and spread wildfire from person to person.”

The mobility of devices and equipment around the hospital underscores the need for more awareness of these items' potential for pathogen transmission, and experts emphasize the importance of raising awareness among healthcare workers that these objects can be highly contaminated.

“Devices and equipment roam all over the facility – that why they are called COWs (computers on wheels). Education should be conducted regularly with all HCPs to raise the awareness of this issue and how to combat it.  Again, emphasize hand hygiene, environmental cleaning, as well as identification and cleaning of fomites.  It may not be too exciting, but it is important.  In many instances, it is a matter of going to specific units and identifying every piece of patient-care equipment and establishing who cleans it, how do they clean, how do they know it is clean, etc.”

Rupp says that some of the tools that can be used to help identify problems is UV-tagged marking gels and ATP detection. “These tools allow one to establish more clearly that surfaces are contaminated or are not being cleaned appropriately,” he says.

“Sometimes, little demonstration projects can be fun and elucidating,” Rupp adds. “Culturing keyboards and posting pictures on a unit of what the culture plates look like; posting pictures of visibly soiled equipment items, and posting data regarding cleanliness of high-touch objects on a ward, are all ways to increase awareness and get a bit of the ‘ick-factor’ working in your favor.”

Some fomites’ role in the transmission of disease is still being debated. Shoe sole and floor contamination is another consideration in the environmental hygiene challenge for healthcare institutions. Research seems to indicate what common sense already tells us -- that items which contact the floor are contaminated and could serve as vectors.

In the now-antiquated Guidelines for Environmental Infection Control in Health-Care Facilities (2003), the CDC asserted, "Extraordinary cleaning and decontamination of floors in healthcare settings is unwarranted. Studies have demonstrated that disinfection of floors offers no advantage over regular detergent/water cleaning and has minimal or no impact on the occurrence of healthcare-associated infections. Additionally, newly cleaned floors become rapidly re-contaminated from airborne microorganisms and those transferred from shoes, equipment wheels, and body substances. Nevertheless, healthcare institutions or contracted cleaning companies may choose to use an EPA-registered detergent/disinfectant for cleaning low-touch surfaces (floors) in patient-care areas because of the difficulty that personnel may have in determining if a spill contains blood or body fluids (requiring a detergent/disinfectant for clean-up) or when a multidrug-resistant organism is likely to be in the environment. Methods for cleaning non-porous floors include wet mopping and wet vacuuming, dry dusting with electrostatic materials, and spray buffing. Methods that produce minimal mists and aerosols or dispersion of dust in patient-care areas are preferred."

The recommendation from the dated CDC guidance is to "keep housekeeping surfaces (floors, walls and tabletops) visibly clean on a regular basis and clean up spills promptly." Additionally, the CDC indicated, "After the last surgical procedure of the day or night, wet vacuum or mop operating room floors with a single-use mop and an EPA-registered hospital disinfectant." These guidelines have not been updated by HICPAC since their issuance.

More recently, Koganti, et. al. (2016) observed, "… hospital floors are often heavily contaminated but are not considered an important source for pathogen dissemination because they are rarely touched. However, floors are frequently contacted by objects that are subsequently touched by hands (e.g., shoes, socks, slippers). In addition, it is not uncommon for high-touch objects such as call buttons and blood pressure cuffs to be in contact with the floor (authors’ unpublished observations)." The authors posited that floors may be an "underappreciated reservoir for pathogen transmission.”

Deshpande, et al. (2017) made a strong argument for a new focus on floors with their survey of five hospitals. They found that floors in patient rooms were frequently contaminated with pathogens and high-touch objects such as blood pressure cuffs and call buttons were often in contact with the floor. Contact with objects on floors frequently resulted in transfer of pathogens to hands.

In this study, researchers cultured 318 floor sites from 159 patient rooms (two sites per room) in five Cleveland-area hospitals. The hospital rooms included both C. difficile infection (CDI) isolation rooms and non-CDI rooms. Researchers also cultured hands (gloved and bare) as well as other high-touch surfaces such as clothing, call buttons, medical devices, linens, and medical supplies. The researchers found that floors in patient rooms were often contaminated with MRSA, VRE, and C. difficile, with C. difficile being the most frequently recovered pathogen found in both CDI isolation rooms and non-CDI rooms. Of 100 occupied rooms surveyed, 41 percent had one or more high-touch objects in contact with the floor. These included personal items, medical devices, and supplies. MRSA, VRE and C. difficile were recovered from 6 (18 percent), 2 (6 percent), and 1 (3 percent), respectively of bare or gloved hands that handled the items.

“Efforts to improve disinfection in the hospital environment usually focus on surfaces that are frequently touched by the hands of healthcare workers or patients,” observe Deshpande, et al. (2017) “Although healthcare facility floors are often heavily contaminated, limited attention has been paid to disinfection of floors because they are not frequently touched. The results of our study suggest that floors in hospital rooms could be an underappreciated source for dissemination of pathogens and are an important area for additional research.”

In their study, Rashid, et al. (2016) implicated the shoes of healthcare personnel as a potential vector. The researchers reviewed the literature to assess the evidence that shoe surfaces are vectors for infectious disease transmission and to evaluate the evidence for the efficacy of disinfectants to decontaminate shoe surfaces.

As the researchers note, "Despite a high likelihood of microbiological contamination, shoes are not often considered a vector for infectious diseases transmission. A search identified no systematic review of this topic … After a thorough bibliographic search, studies were identified that showed high rates of bacterial shoe sole contamination in the hospital-, community, and animal worker areas. Although several chemical and nonchemical decontamination strategies have been tested, none have shown to be able to consistently decontaminate shoe bottoms."

They comment further, "In this review, many of the most common microbiologic pathogens including MRSA, Enterococcus, Cl. difficile, and Gram-negative bacteria were identified on shoe soles. Disease transmission of MRSA has been shown to be increased in hospitals with increased patient sharing between hospitals as opposed to hospitals that do not share patients (Chang, et al. 2016). Movement of MRSA from hospital to hospital was commented to be likely due to patient spread; however, it is possible that shoe bottoms could have also accounted for the vector spread based on findings from this meta-analysis. All these hypotheses will require generation of a transmission dynamic model from the bottoms of shoes to a patient. All of these data should be tested in the context of proper handwashing and other proven infection control practices."

As Rashid and VonVille, et al. (2016) observe, "From the floor, it is plausible that air currents, human movements over the floor and other factors that aerosolize or provide an airborne opportunity for the organism may occur, thus causing human infections via inhalation, horizontal or cross-contamination from other persons, clothing or equipment that the organism resettles upon. It is furthermore plausible that due to the existence of these microbiological pathogens on shoe soles that the rapid spread of these organisms in the healthcare environment can be directly related to the organisms on floors getting picked up and carried by shoe soles and retransferred to floors in other areas by human movement. This potential transmission dynamic requires validation. Shoes become contaminated from a dirty floor and parallel methods to decontaminate flooring is also required. Perhaps most surprising finding from this study was the relative lack of consistent efficacy to decontaminate shoe bottoms using either chemical or nonchemical strategies. Although, most strategies had variable success, the complexity of maintaining sterility of the disinfectant strategy appeared to be the most complex and difficult to optimize component of the decontamination strategy. For example, Langsrud, et al. (2006) reported that chlorine-containing foo baths may act as a source of bacterial contamination in food factories. Taken together, these results suggest the shoe soles can be a likely vector for infectious diseases transmission and an effective decontamination strategy is direly needed."

As Mustapha, et al. (2018) summarize, "As has been reported previously, we found that floors in patient rooms prior to post-discharge cleaning were frequently contaminated with important health care–associated pathogens. We demonstrated that manual post-discharge cleaning by EVS personnel in our facility significantly reduced floor contamination with MRSA, Candida spp, and C difficile.” They continue, "One caveat of our findings is that the efficacy of manual cleaning in reducing floor contamination is likely to vary with different cleaning products and with differences in the quality of cleaning by EVS personnel. In our facility, ongoing interventions are in place to monitor and improve cleaning performance by EVS personnel. In addition, floors are mopped with a quaternary ammonium–based disinfectant and mop heads are changed between rooms. In contrast, Wong et al. demonstrated that aerobic colony counts on floors increased after manual cleaning when a neutral detergent was used, and the solution and mop head were only changed after every third room. Although we found that manual cleaning resulted in a reduction in C. difficile floor contamination, the reduction must be attributable to mechanical removal because quaternary ammonium disinfectants have no activity against spores. If mop heads are not changed between rooms, spores could easily be transferred from room to room."

Kraay, et al. (2018) emphasize that “Fomite-mediated transmission can be an important pathway causing significant disease transmission… The importance of these pathways relative to other transmission pathways such as direct person-person or airborne will depend on the characteristics of the particular pathogen and the venue in which transmission occurs.” In their study, the researchers developed and analyzed a compartmental model that accounts for fomite transmission by including pathogen transfer between hands and surfaces. They focused on two sub-types of fomite-mediated transmission: direct fomite (e.g., shedding onto fomites) and hand-fomite (e.g., shedding onto hands and then contacting fomites). They used this model to examine influenza, rhinovirus and norovirus in four venue types.

As the researchers explain, “Transmission venues are complex environments characterized both by their physical properties (types and quantity of fomites) and by the nature of host behaviors within these spaces (frequency of contact with fomites, the duration of time spent in a venue, or the density of hosts within the venue). Furthermore, risk within a venue may also vary by age group based on not only differences in contact rates but also shedding rates.”

For their analysis, the researchers used a simplified representation of a venue, based on three factors: the proportion of contamination-accessible fomites, shedding rates, and how frequently individuals interact with those fomites. For this analysis, the researchers treated each venue as a closed system and did not consider host movement. They included control measures parameters (cleaning rate and the proportion of pathogens killed by decontamination) to contrast the effectiveness of control measures among the pathogens and across venues. They considered three frequencies for all three venues: 1/2 days, daily, and twice daily.

The researchers considered two behavioral parameters: the rate of self-innoculation (face-touching events) and the rate of fomite touching. They found that for all pathogens, the inactivation rates on fomites were highly variable by surface, with higher inactivation rates on hands (which are a porous surface): “Influenza, the only pathogen for which decay rates were available for porous environmental surfaces besides stainless steel, had much higher inactivation rates on porous surfaces. Notably, some pathogens exhibited biphasic inactivation, with faster initial inactivation followed by a period of slow inactivation or persistence without measurable decay. When this occurred, we used the average inactivation estimates over the first hour, when decay rates were highest, to parameterize our model. Influenza appears to survive for the shortest amount of time on hands, with an order of magnitude higher inactivation rate than either rhinovirus or norovirus. While inactivation rates on fomites were relatively insensitive to temperature, they were more sensitive to changes in humidity, with drier conditions generally promoting higher inactivation rates. The exception was influenza, which appeared to survive better at low humidity.”

The researchers discovered that influenza transfers more readily from fomites to hands than hands to fomites, while the reverse appears to be true for norovirus. For influenza, transfer efficiency was also lower for porous than non-porous surfaces.

Shedding concentrations varied considerably between pathogens as well as between individuals for a given pathogen, the researchers reported. The average shedding rate for influenza was found to be an order of magnitude higher than for rhinovirus and norovirus.

Behavior and venue are important drivers of transmission, Kraay, et al. (2018) emphasize. For influenza, transmission via the fomite route is only sustainable for venues with high touching rates, they say: “Airborne transmission may therefore be more likely to sustain influenza transmission in venues where either the touching rate is low (offices) or proportion of accessible surfaces is very low (outdoor venues). By contrast, our model suggests that rhinovirus and norovirus transmission by the fomite pathway are sustainable in nearly all venues. While norovirus and rhinovirus shed fewer viral copies than influenza, they have much longer infectious periods, as well as longer persistence on hands.”

The direct fomite route is most important for transmission of influenza, the researchers found, whereas the hand-fomite route was more important for rhinovirus and norovirus: “Based on our sensitivity analyses, for norovirus and influenza, the relative importance of each pathway was highly sensitive to the fraction of pathogens shed onto hands rather than surfaces. When a larger proportion of pathogens was shed onto surfaces, the direct fomite route became more important. The reason the hand-fomite route dominated for rhinovirus is due to its relatively larger transfer efficiency proportion and low inactivation rate on hands.”

For influenza, only higher frequency (≥ 1/day) surface decontamination strategies appear to meaningfully reducing transmission, with a maximum reduction of 40 percent in low surface-contact venues. However, fomite transmission is only possible in settings with higher touching rates and proportions of accessible surfaces. Thus, surface decontamination for influenza may prevent outbreaks in venues with moderate surface contact rates and many accessible surfaces, the researchers say. In contrast, in the researchers’ simulations similar interventions for rhinovirus and norovirus were not effective, even with cleaning frequencies of up to twice per day.

The researchers indicate that it may be important to tailor environmental interventions to specific venues, “as the effect of a given influenza transmission mechanism may not be consistent between venues with different environmental properties … To be effective, surface decontamination interventions for norovirus and rhinovirus may need to be more frequent (more than once a day), tailored to the specific context, and timed early in outbreaks to interrupt transmission. These differences were driven by the interaction between multiple properties of the pathogens. Because of its low transfer efficiency, high inactivation rates on hands, and relatively short duration of infectiousness, influenza had the lowest R0 for the fomite route, making fomite-mediated transmission easier to control despite its high shedding rate. Both rhinovirus and norovirus were more efficiently transferred, had high persistence on both hands and fomites, and produce longer periods of shedding, making the transmission potential high for both pathways and consequently more difficult to control, even with frequent surface decontamination.”

They conclude, “Fomite-mediated transmission introduces both challenges and opportunities for infection control due to interactions between the properties of pathogens and venues. Our analysis has shown that fomites can be an important source of risk for pathogens that are often considered to be, primarily, directly transmitted. We found that fomite-mediated transmission is dependent on both behavioral factors influencing contact with fomites as well as the physical environment and surfaces available for contamination in each venue. This result underscores the need to think critically about how a venue is characterized from a transmission perspective in order to design interventions that can appropriately target key stages in the transmission process.”

The criticality of cleaning and disinfecting fomites is underscored when considering the ubiquitous use of portable medical equipment (PME) in the hospital setting. Who cleans PME and how often was investigated by Chetan Jinadatha, MD, MPH, clinical associate professor at the Texas A&M Health Science Center College of Medicine and chief of infectious diseases at the Central Texas Veterans Health Care System in Temple, Texas, who, with his co-authors, examined the patterns and sequence of touch events among healthcare workers, patients, surfaces and equipment in the hospital environment to better inform their understanding of potential infection transmission pathways.

As Jinadatha, et al. (2017) explain, "High-touch surfaces in the hospital environment, such as bed rails, tray tables, and supply carts, are considered important in the epidemiology of transmission of healthcare-associated infections (HAIs). If not removed adequately, pathogens can remain viable on fomites for months, serving as a source of transmission on a number of susceptible patients."

Jinadatha, et al. (2017) conducted their study on six inpatient units, performing continuous 24-hour observation separately on each unit by two research team members observing for eight-hour sessions. Observations of healthcare workers’ touches of surfaces, patient, and objects were recorded in sequence. The researchers found that almost all the items touched were connected to at least a few other items in a sequence of touches. The patient, the most commonly touched item, had a potential for contamination from other surfaces as well as a potential for transmitting pathogens to other surfaces.

The study data included the surface/medical equipment touched; the order of touches; what the equipment was used for in that interaction (such as a surface work area for IV fluids or medications); whether equipment entered or exited the room – to determine if the equipment is patient dedicated or shared; if disinfection of equipment or surfaces took place at any time during this interaction; and if hand hygiene was performed.

Jinadatha and colleagues note that their results demonstrated that PME such as a computer on wheels and IV pump were two of the most highly touched items during patient care. Even with proper hand sanitization and personal protective equipment, this sequence analysis reveals the potential for contamination from the patient and environment, to a vector such as portable medical equipment, and ultimately to another patient in the hospital.

As Jinadatha, et al. (2017) note, "Most PME falls under the noncritical patient care device category of the Spaulding Classification Scheme for infection risk. The disinfection of equipment, along with room high-touch surfaces, is one of the highest priorities in the current Joint Commission scores with high non-compliance issues. The CDC recommends that noncritical patient-care devices be cleaned on a regular basis but the recommendations are based on time since the last cleaning rather than how frequently the PME is touched/used. For example, the CDC recommends that a computer on wheels (COW) be cleaned once a day or as needed, or an IV pump cleaned following patient discharge or disuse. If contact events or 'touches' are a means of spreading contamination across surfaces in the environment, then cleaning recommendations based on number of touches may be more effective than those based on the passage of time. However, while existing data on touch frequency have helped to identify high-touch surfaces in the patient care environment, it is difficult to continuously track the patterns of touches. Further research is necessary to quantify the degree of surface contamination associated with touch activity."

Other researchers are equally concerned about the role that PME may play in transmitting healthcare-associated infections (HAIs). Suwantarat, et al. (2017) demonstrated that hospitalized patients frequently interact with shared equipment, and these items were often contaminated, and they emphasize that there is a need for protocols to ensure routine cleaning of shared portable equipment. As the researchers acknowledge, "Efforts to improve environmental disinfection in healthcare facilities typically focus primarily on surfaces in patient rooms that are frequently touched by healthcare workers and patients (bed rails, bedside tables). Portable equipment that is shared among patients (e.g., medication carts, vital signs equipment, wheelchairs, electrocardiogram machines) can also be a potential source of pathogen transmission. Therefore, current guidelines recommend that medical equipment that contacts intact skin is cleaned and decontaminated after each patient use. In clinical practice, nursing staff and ancillary staff are often given responsibility for cleaning portable equipment because they use such equipment while working with patients. However, Havill, et al. (2011) reported that portable equipment was often not cleaned according to written protocols between each patient use."

Healthcare textiles and other soft surfaces may also play a role in the transmission of infectious agents. An increasing number of experts are investigating these contaminated textiles (including privacy curtains, upholstery, apparel, etc.) as a vehicle for cross-contamination and transmission of multidrug-resistant organisms (MDROs). Studies indicate that microorganisms shed by patients can contaminate hospital surfaces at concentrations sufficient for transmission, and that these pathogens survive and persist for extended periods despite attempts to disinfect or remove them and can be transferred to the hands of healthcare personnel.

As Mitchell, et al. (2015) note, "…while considerable effort is placed on cleaning and disinfection of non-porous or high-touch environmental surfaces, much less effort is placed on the procedures for cleaning and decontaminating porous, soft surfaces or healthcare textiles (privacy curtains, linen, upholstery, patient furniture or room furnishings) … The complex role that these textiles play in acquisition and retention of pathogens is further complicated by varied laundering conditions and requirements. While the CDC and agencies … provide guidance for laundering contaminated textiles, achieving optimal water temperature, drying time and dedicated process flow can be difficult to achieve in healthcare facilities, and nearly impossible in homes."

Without timely intervention, privacy curtains in hospitals can become breeding grounds for resistant bacteria, posing a threat to patient safety, say Shek, et al. (2018) who conducted a study which tracked the contamination rate of 10 freshly laundered privacy curtains. While the curtains had minimal contamination when they were first hung, the curtains that were hung in patient rooms became increasingly contaminated over time – and by day 14, 87.5 percent of the curtains tested positive for MRSA. In contrast, control curtains that were not placed in patient rooms stayed clean the entire 21 days. None of the rooms where the curtains were placed were occupied by patients with MRSA. Four curtains were placed in a four-bed room; four were placed in two double rooms; and two controls were placed in areas without direct patient or caregiver contact. Researchers took samples from areas where people hold curtains, suggesting that the increasing contamination resulted from direct contact.

“We know that privacy curtains pose a high risk for cross-contamination because they are frequently touched but infrequently changed,” says Kevin Shek, BSc, the study’s lead author. “The high rate of contamination that we saw by the 14th day may represent an opportune time to intervene, either by cleaning or replacing the curtains.” By day 21, almost all curtains exceeded 2.5 CFU/cm.

References:

Deshpande A, et al. Are hospital floors an underappreciated reservoir for transmission of healthcare-associated pathogens. Am J Infect Cont, 2017; 45: 336-338.

Havill NL, et al. Cleanliness of portable medical equipment disinfected by nursing staff. Am J Infect Control, 39; Pp. 602-604. 2011.

Jinadatha C, et al. Interaction of healthcare worker hands and portable medical equipment: a sequence analysis to show potential transmission opportunities. BMC Infectious Diseases. 2017;17:800.

Kanamori H, et al. The Role of Patient Care Items as a Fomite in Healthcare-Associated Outbreaks and Infection Prevention. Clin Infect Dis. Vol. 65, No. 8, Pp. 1412-1419. October 2017.

Koganti, et. al. Evaluation of hospital floors as a potential source of pathogen dissemination using a nonpathogenic virus as a surrogate marker. Infect Cont & Hosp Epidemiol, 2016: 37 (11): 1374-1377.

Kraay ANM, et al. Fomite-mediated transmission as a sufficient pathway: a comparative analysis across three viral pathogens. BMC Infect Dis. 18: 540. Oct. 29, 2018.

Messina G, et al. How many bacteria live on the keyboard of your computer? Am J Infect Control. 39(7):616-8. Sept. 2011.

Mitchell A, et al. Role of healthcare apparel and other healthcare textiles in the transmission of pathogens: a review of the literature. J Hosp Infect, 90; Pp. 285-292. 2015.

Mustapha A, et al. Efficacy of manual cleaning and an ultraviolet C room decontamination device in reducing healthcare-associated pathogens on hospital floors. Am J Infect Control. May;46(5):584-586. 2018.

Rashid T, et al. Shoe soles as a potential vector for pathogen transmission: a systematic review. J Appl Microbiol. Nov;121(5):1223-1231. 2016.

Shek K, et al. Rate of contamination of hospital privacy curtains in a burns/plastics ward: A longitudinal study. Am J Infect Control. Vol. 46, No. 9. September 2018.

Simmonds R, et al. Mobile phones as fomites for potential pathogens in hospitals: microbiome analysis reveals hidden contaminants. J Hosp Infect. Oct. 1, 2019.

Suwantarat N, et al. Quantitative assessment of interactions between hospitalized patients and portable medical equipment and other fomites. Am J Infect Control. Vol. 45, No. 11. Pages 1276-1278. November 2017.

Xiao S, et al. The dynamic fomite transmission of Methicillin-resistant Staphylococcus aureus in hospitals and the possible improved intervention methods. Building and Environment 161:106246. July 2019.

Recommended reading:

Huslage K, et al. A quantitative approach to defining “high-touch” surfaces in hospitals. Infect Control Hosp Epidemiol, 31 (2010), pp. 850-853.

Weber DJ, et al. The role of the surface environment in healthcare-associated infections. Curr Opin Infect Dis. 2013; 26:338-44.

Otter JA, et al. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol. 2011; 32:687-99.