Experts Ponder the Big Issues in Environmental Hygiene

What happens when some of the brightest minds in epidemiology and infectious disease convene to discuss and debate some of the toughest issues in environmental hygiene and infection prevention? The gathering raises more questions than answers but establishes a firmer footing in the research agenda to help further address current challenges. In May, the Society for Healthcare Epidemiology of America (SHEA) held its spring conference and included "Advancing Healthcare Epidemiology and the Role of the Environment" as one of several tracks exploring imperatives in epidemiology.

By Kelly M. Pyrek

Editor's note: For more perspectives from SHEA's spring conference, look for a special Pulse digital issue available HERE.

What happens when some of the brightest minds in epidemiology and infectious disease convene to discuss and debate some of the toughest issues in environmental hygiene and infection prevention? The gathering raises more questions than answers but establishes a firmer footing in the research agenda to help further address current challenges. In May, the Society for Healthcare Epidemiology of America (SHEA) held its spring conference and included "Advancing Healthcare Epidemiology and the Role of the Environment" as one of several tracks exploring imperatives in epidemiology. Let's explore the various ideas and perspectives coming out of this meeting.

In the presentation, "The Role of the Inanimate Environment in Healthcare-Associated Infections: History, Current Knowledge, Future Challenges," Stephanie Dancer, BSc, MBBS, MD, MSc, FRCPath, DTM&H, FRCP(Ed), delivered a rousing talk exploring the issues with which practitioners grapple, including the fact that environmental hygiene has weaker evidence compared to other sciences. She pointed to an excerpt from a 2012 lecture by Stephen Harbarth that noted, "Traditional environment-based hospital hygiene has long been considered a weak science... usually arising from the creation of a global hypothesis... poetically elaborated upon by its creator ... without any appeal to patient-oriented facts that would be capable of confirming or refuting it."  But Dancer emphasized that will change and that "It's all about the cleaning." She cautioned that the history of hygiene has a legacy in the "shiny floor syndrome" and that patients' and practitioners' views on cleanliness are a swinging pendulum. Dancer says we are still debating the role of the environment in HAIs for many reasons, including the obvious fact that pathogenic microorganisms are invisible, because there are aesthetic biases to conquer, pathogen detection is challenging; and there are no widely accepted methods of measurement based in science currently. For example, Dancer points to patients' nonevidence-based perceptions that are associated with objective measures of hospital quality (Graves, et al. 2012).

Dancer reviewed various studies in the literature regarding the role that hand-touch surfaces (both patients and healthcare workers) play in the HAI discussion, and emphasized that cleaning these sites and the frequency of the cleaning are just as important as cleaning hands. She pointed to Stiefel, et al. (2011) who found that hand contamination with MRSA was the same after contact with patients' skin and frequently touched sites in patient rooms. She also touched upon the issue of colonized prior-room occupants that can leave behind pathogenic organisms if rigorous cleaning and disinfection is not performed, emphasizing that it is just as easy to pick up microbes from the environment as it is form the patient. Dancer also addressed the transmission cycle of hospital pathogens, consisting of patients, caregivers' hands and the environment, exploring which comes first, the patient or the environment -- she suggested that patients' hands may be the so-called missing link in terms of closing the infection control loop.

Dancer also tackled the issue of measuring cleaning effectiveness, noting the study by Griffith, et al. (2000) which said that "clean" is whatever an individual thinks it is. She indicated that a majority of hospitals are still measuring cleanliness with a visual inspection, while a smaller percentage is relying on surfaces being microbiologically clean and still a smaller percentage who rely on a method such as ATP.  Dancer reviewed the various methods used to indicate bioload left on surfaces that have been cleaned, specifically surface evaluation using ATP bioluminescence, where a swab is used on a surface, there is luciferase tagging of ATP by way of a luminometer that provides ATP values in relative light units (RLUs) (Mulvey, et al., 2011). Dancer acknowledged that microbiological standards could help practitioners better determine levels of bioload in a time of disagreements about RLUs. In a 2004 paper, Dancer proposed microbiological standards for surface hygiene in hospitals:
- standard 1: There should be <1cfu/cm(2) pathogen in the clinical environment
- standard 2: Aerobic colony count or total microbial growth level from a hand contact surface should be <5cfu/cm(2)

In terms of applying cleaning standards in a high-risk environment such as an intensive care unit (ICU), Dancer pointed to studies indicating that as much as 25 percent of 200 samples -- mostly hand-touch sites -- failed the standards. These hygiene failures were associated with bed occupancy and incidence of ICU-acquired infection; the study authors indicated that hygiene standards reflect patient activity and provide a means to manage infection. Mulvey (2011) showed hygiene failures for three ATP benchmarks according to microbial growth, while Lewis, et al. (2008) showed a relationship between aerobic colony count and its pass or fail using ATP levels or visual assessment (and ATP reflected greater failure rates). Dancer noted that when using ATP to identify hygiene failures, the benchmark must be chosen with great care.
Dancer circled back to the hand-touch equation, exploring why all of the emphasis is placed in hand cleaning and not on the surfaces that hands touch.  She emphasized the need for better manual cleaning and disinfection and noted that the most successful cleaning interventions share their root in some form of performance monitoring and observation, whether it be supervision, covert fluorescent tagging of surfaces and objects in rooms, or feedback and education. She also covered the need for continual cleaning, pointing to various studies indicating that hospital surfaces become recontaminated fairly quickly after cleaning. As Dancer noted, once-a-day cleaning is the bare minimum because nature abhors a vacuum -- pathogens return very quickly. So, the bottom line is that killing of pathogens coupled with physical removal is critical int he fight against HAIs, and she cited Speight, et al. (2011) who found that a single cleaning can reduce contamination by about 90 percent.

To sum up, Dancer noted that for modern cleaning, what works best is detergent over disinfectants, used in targeted ways, and done frequently, as well as practical standards for surface level cleanliness in hospitals that reflect critical risks.

In his presentation, "Role of Inanimate Surfaces and Fomites in Transmission of Nosocomial Pathogens," Daniel Morgan, MD, MS, reviewed the complicated transmission cycle between one patient to the next within the context of how pathogenic organisms are carried, transferred and recycled among healthcare workers who touch not only the patients but the contaminated objects and surfaces in the patient rooms. In terms of the concept of a hospital microbiome, Morgan emphasized that almost nothing is sterile, and that the microbiology of the healthcare environment is not completely understood well. He reviewed what constitutes common fomites in the hospital environment, such as computer keyboards, portable electronic equipment, stethoscopes, cell phones, blood pressure cuffs, in addition to items in the vicinity of the patient, along with dozens of other items. He noted that while the hospital cannot be sterile overall, it is concerning that it is still not known just how much contamination is necessary for the transmission of infection and that it makes sense to ensure proper cleaning of fomites. He noted that room contamination is generally understood, relating to the patient's bacteria as opposed to "foreign" bacteria (Dumford, et al., 2009 conducted a survey of surfaces outside of the patient room for C. difficile and found 31 percent of physician work areas to be contaminated; 10 percent in nursing areas; 26 percent of desktop computers; 100 percent of doorknobs; and 33 percent of portable computers), and that numerous pathogens can persist for significant amount of time. 

Morgan reviewed the choice available for reducing contamination in the environment, including manual cleaning and disinfection, touchless technology and automated technology (such as HPV and UV) that can be used for adjunct cleaning; as well as changing the environment itself through the use of antimicrobial surfaces such as copper -- with the caveat that surfaces must still be cleaned because the build-up of bioburden can reduce the effect of the antimicrobial surface. Morgan pointed to research by Lin and Hayden (CCM, 2010) that showed room contamination can spread contamination to healthcare workers through touch and apparel. Morgan summarized that although studies show that healthcare worker contamination is common, there is scant data to suggest that this contamination can lead to patient transmission. He suggested that healthcare professionals keep track of fomites and know how to clean them or use dedicated items; perfect the basic environmental cleaning practices; spend more resources, time and money on the pathogens of particular concern in the hospital; and don't forget about hand hygiene and the use of barrier precautions.

In his presentation, "Everything You Need to Know About Culturing the Environment," John Boyce, MD, emphasized the need for the input of infection preventionists when performing routine culturing of the environment. He advised that this kind of sampling be conducted in outbreak investigations or as part of the monitoring of cleaning and disinfection practices. He acknowledged that although there are dozens of methods that have been used by investigators for culturing the environment in healthcare settings, there is no widely accepted criteria for defining surfaces as "clean"  and the that the level of contamination needed to prevent transmission is not known. Boyce reviewed the most common methods for culturing environmental surfaces, including swabs, wipes and direct immersion, as well as RODAC plates. He also reviewed the advantages and disadvantages of each method, and then outlined the factors that can affect the results of each method. For example, in the swab-based cultures, factors include the type of swab used (cotton vs. nylon), the wetting solution used, twirling of the swab, swabbing pattern and surface area sampled. Boyce indicated that using moistened swabs with direct plating of solid agar is easy to perform, yields useful semi-quantitative results, but is the least sensitive method for detecting microorganisms. He added that moistened swabs and rinse method is more sensitive than direct plating; it will detect lower levels of bacterial contamination; it also yields qualitative results due to incubation of broth before plating. Wipe-rinse and sponge-rinse methods are useful for sampling larger areas, and are more sensitive than swab-based methods due to larger area sampled. It requires more laboratory equipment and processing the swabs. Culturing flat surfaces using RODAC plates is easy to perform, samples a defined area, and provides quantitative results. It is currently the more standardized approach to quantifying levels of bacterial contamination of surfaces; it is preferable to use neutralizer-containing plates if residual disinfectant is likely to be on surfaces.

In her presentation, "How Should We Measure Hospital Cleaning?" L. Silvia Munoz-Price, MD, reviewed the recommendations from the CDC on a tiered hospital cleaning program (Guh and Carling, 2010) which recommends the optimization of cleaning practices, staff education, as well as objective monitoring. She also reviewed the well-known studies by Carling and colleagues that reported on use of a novel assessment tool after finding subpar cleaning in hospitals.

She also reviewed a project conducted in her hospital that examined different approaches to monitoring cleaning and the staff members' reactions to them. For example, there was concern and confusion about who would clean sensitive patient-care equipment  such as IV pumps, and it was eventually decided that nursing and environmental services personnel were responsible for cleaning certain objects. The project revealed other staff concerns, such as whether a bioluminescent substance used as a marker could really equate to bacteria left behind after cleaning, and that was addressed by making something subjective into something more objective by using ATP.  Some staff began buying their own black lights to find the markers and Munoz-Price emphasized to them that the point was to clean the surfaces and objects, and not merely remove the markers. Munoz-Price said that with markers plus cultures, it was harder for staff to argue that objects are not cleaned adequately and recontamination keeps occurring. In the end, the hospital stopped providing feedback on a weekly basis; currently they only conduct environmental surveillance as needed and in conjunction with environmental cultures.

Munoz-Price pointed to the question of whether improving terminal cleaning in the OR impacts surface contamination with bacterial pathogens. She reported on the OR Environmental Hygiene project conducted at University of Miami Jackson Memorial Hospital, "Decreasing OR Environmental Pathogen Contamination Through Improved Cleaning Practice." Because potential transmission of organisms from the environment to patients is a concern, especially in enclosed settings, such as operating rooms, in which there are multiple and frequent contacts between patients, provider's hands, and environmental surfaces. Therefore, adequate disinfection of operating rooms is essential. Munoz-Price, et al. (2012) aimed to determine the change in both the thoroughness of environmental cleaning and the proportion of environmental surfaces within operating rooms from which pathogenic organisms were recovered. Their project was a prospective environmental study using feedback with UV markers and environmental cultures, conducted in a 1,500-bed county teaching hospital. Study participants included environmental service personnel, hospital administration, and medical and nursing leadership. The proportion of UV markers removed (cleaned) increased from 0.47 (284 of 600 markers) at baseline to 0.82 (634 of 777 markers) during the last month of observations. The researcher report that the percentage of samples from which pathogenic organisms (gram-negative bacilli, Staphylococcus aureus, and Enterococcus species) were recovered did not change throughout the study. Pathogens were identified on 16.6 percent of surfaces at baseline and 12.5 percent of surfaces during the follow-up period; however, the percentage of surfaces from which gram-negative bacilli were recovered decreased from 10.7 percent at baseline to 2.3 percent during the follow-up period. Munoz-Price, et al. (2012) concluded that feedback using Gram staining of environmental cultures and UV markers was successful at improving the degree of cleaning in operating rooms.

In his presentation, "Developing the Best Paths to Improved Thoroughness of Cleaning," Mark Rupp, MD, reported on a study, "The Time Spent Cleaning a Hospital Room Does Not Correlate with the Thoroughness of Cleaning," in which he and colleagues demonstrated improved cleaning of high-touch surfaces through the use of a fluorescent marking solution and rapid-cycle performance feedback.As part of an earlier study, housekeepers were instructed about the importance of environmental cleanliness and appropriate cleaning of high-touch surfaces, and a room cleaning checklist was introduced. In this study, the researchers sought to examine the relationship between the amount of time that a housekeeper spent cleaning a hospital room and the thoroughness of surface cleaning.

The project was conducted in four adult medical-surgical critical care units (unit AD) with 74 beds during December, 2008, and January, 2009. Fifteen high-touch surfaces in each critical care room were covertly marked by study personnel with a transparent, water-soluble solution that fluoresces when exposed to UV light. The high-touch surfaces consisted of the room door handle, thermometer, patient monitor, bedside tray table, bedrails and release buttons, nurse call box, faucet handle, computer mouse, light switches, cabinet handle, and hand gel dispenser handle. Environmental service personnel were not responsible for cleaning three of the surfaces (the thermometer, monitor, and computer mouse). After discharge of the patient from the hospital and routine terminal cleaning of the room, the high-touch surfaces were surveyed by study personnel, and the rooms were scored according to the percentage of surfaces appropriately cleaned. Twenty-four different housekeepers were involved, and their identities were not recorded as part of the project. The amount of time spent by housekeepers to clean a room was monitored through use of an automated system that required personnel to document by telephone when they arrived at the room and when room cleaning was complete.

Six hundred high-touch surfaces were marked in 40 critical care rooms (10 rooms per unit). Cleaning thoroughness ranged from a low of 5% for the monitor to a high of 79 percent for the computer mouse. Cleaning of high-touch surfaces was similar from unit to unit except for the room door handle (which was cleaned less well in unit B; ) and cabinet handle (which was cleaned less well in units B and D; ). The room cleaning checklist was completed less frequently in unit C (30 percent completion) than in the other three units (60 percent to 90 percent completion; ). However, the median number of surfaces cleaned was similar for a room whether the checklist was completed or not. The overall thoroughness of cleaning (percentage of high-touch surfaces cleaned) was 41 percent and ranged from 33 percent to 51 percent among intensive care units. Specific room cleanliness ranged from a low of 0 percent to a high of 80 percent. There was no significant correlation between the thoroughness of cleaning high-touch surfaces (with or without consideration of the three surfaces that housekeepers were not responsible for cleaning) and the amount of time required to clean the room. There was a wide discrepancy between thoroughness and efficiency. Although a few rooms were fairly well cleaned within 30 minutes (which is an accepted industry benchmark), many of the rooms with below-average cleaning took considerably longer to clean.

As Rupp, et al. (2013) explain, "Unexpectedly, there was no correlation between the amount of time spent cleaning a room and the thoroughness of cleaning high-touch surfaces as documented by the UV-tagged marking system. This finding has important implications for institutions that devise strategies to optimize cleaning. Our study lends support to and may explain earlier studies that have shown that improved cleaning performance can be achieved without substantial additional cost. Clearly, adequate time must be allotted for personnel to clean a room properly, but it is apparent that additional time taken to clean a room is no guarantee of adequate cleaning. These data also support additional evaluation to discern whether an optimum outlier (positive deviance) process improvement program could be employed to improve environmental cleanliness. Because several of the environmental service staff in our study appear to be optimum outliers and are able to clean hospital rooms quickly and thoroughly, they may be able to provide personal and programmatic insights to explain their proficiency and serve as models for their coworkers." The researchers concluded that their findings emphasize that process improvement interventions should evaluate both the efficiency and thoroughness of hospital surface cleaning to optimize the cost effectiveness of cleaning practice in healthcare settings.

In her presentation, "Understanding Attitudes and Beliefs to Optimize Hygienic Practice, " Anne Matlow, MD, shared results of a survey designed to elicit perspectives about their work from environmental services professionals. Matlow, et al. (2012) say that hospital environmental service workers (ESWs) play an important role in interrupting the chain of infection because the environment is a reservoir for nosocomial pathogens. Improving ESWs' knowledge through education has been shown to improve ESW cleaning, but the behavioral determinants of their work have not been studied. Understanding and targeting ESWs' attitudes and beliefs may inform strategies to improve environmental cleaning. With the theory of planned behavior as framework, the researchers used questionnaires and focus groups to examine intensive care unit ESWs' attitudes, beliefs [behavioral, normative, and control], and control) and intent about their job. Baseline quantitative microbial cultures of high-touch services were performed before and after cleaning. After an educational intervention addressing their attitudes, beliefs, and general infection control knowledge, attitudes, beliefs, and microbial contamination were reassessed. According to Matlow, et al. (2012), beliefs were uniformly strong, and normative beliefs correlated best with intent to clean.

Themes elicited from the focus groups included "me versus them," lack of ap-preciation, pride in work, and "if it were me." The rate of environmental contamination was significantly improved after the intervention (P = .0074 vs P = .0023, respectively); the measured relationship among attitudes, beliefs, and intent was not significantly changed.

Matlow found the following:
- 37 percent said they did not think the environment had germs that can cause disease
- 100 percent thought their work was instrumental in upholding patient safety
- 75 percent thought it mattered to patients if they did a great job
- 100 percent intended to clean well
Matlow emphasized that the focus groups revealed a lack of respect for ESWs, yet they took pride in their jobs and were motivated by wanting cleanliness if they were the patient. She emphasized that attitudes and beliefs do impact cleaning efficacy and providing instruction and motivation can help boost performance.



Matlow AG, Wray R, Richardson SE. Attitudes and beliefs, not just knowledge, influence the effectiveness of environmental cleaning by environmental service workers. Am J Infect Control. 2012 Apr;40(3):260-2. doi: 10.1016/j.ajic.2011.02.024. Epub 2011 Jul 13.

Munoz-Price LS, Birnbach DJ, Lubarsky DA, Arheart KL, Fajardo-Aquino Y, Rosalsky M, Cleary T, Depascale D, Coro G, Namias N, Carling P. Decreasing operating room environmental pathogen contamination through improved cleaning practice. Infect Control Hosp Epidemiol. 2012 Sep;33(9):897-904. doi: 10.1086/667381. Epub 2012 Jul 24.

Rupp ME, Adler A, Schellen M, Cassling K, Fitzgerald T, Sholtz L, Lyden E and Carling P. The Time Spent Cleaning a Hospital Room Does Not Correlate with the Thoroughness of Cleaning. Infect Control Hosp Epidem. 2013.