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. Author manuscript; available in PMC: 2023 Mar 1.
Published in final edited form as: Am J Infect Control. 2022 Mar;50(3):289–294. doi: 10.1016/j.ajic.2021.11.014

Hygienic monitoring in long-term care facilities using ATP, crAssphage, and human noroviruses to direct environmental surface cleaning

Jennifer L Cannon a,b,c,*, Geun Woo Park c, Benjamin Anderson b, Cortney Leone d, Morgan Chao d, Jan Vinjé c, Angela M Fraser d
PMCID: PMC8903150  NIHMSID: NIHMS1771547  PMID: 35184878

Abstract

Background:

Norovirus and C. difficile are associated with diarrheal illnesses and deaths in long-term care (LTC) facilities and can be transmitted by contaminated environmental surfaces. Hygienic monitoring tools such as adenosine triphosphate (ATP) bioluminescence and indicators of fecal contamination can help to identify LTC facility surfaces with cleaning deficiencies.

Methods:

High-touch surfaces in 11 LTC facilities were swabbed and tested for contamination by norovirus, a fecal indicator virus, crAssphage, and ATP which detects organic debris. High levels of contamination were defined as log ATP relative light unit (RLU) values or crAssphage log genomic copy values in the 75th percentile of values obtained from each facility.

Results:

Over 90% of surfaces tested positive for crAssphage or gave failing ATP scores. Norovirus contamination was not detected. Handrails, equipment controls, and patient beds were four times more likely than other surfaces or locations to have high levels of crAssphage. Patient bed handrails and tables and chairs in patient lounges had high levels of both ATP and crAssphage.

Conclusions:

Surfaces with high levels of ATP and crAssphage were identified. Quantifying levels of contamination longitudinally and before and after cleaning might enhance infection prevention and control procedures for reducing diarrheal illnesses in LTC facilities.

Keywords: hygiene monitoring; long-term care; ATP; crAssphage, norovirus; environmental hygiene; C. difficile, Clostridioides difficile; CDI, C. difficile infection; LTC, long-term care; ATP, adenosine triphosphate; PCR, polymerase chain reaction; RT-PCR, reverse transcriptase PCR

Background

Diarrheal illness outbreaks caused by norovirus or C. difficile infections (CDI) are among the most frequent healthcare-associated infections in long-term care (LTC) facilities (1). Approximately 60% of norovirus outbreaks and over half of all healthcare-associated CDI in the US occur in LTC facilities (1, 2). Persons over 65 years of age experience the highest morbidity and mortality due to noroviruses and CDI (3, 4). This creates a prevention challenge for LTC facilities, particularly when compounded by the risks associated with comorbidities among the residents, close living arrangements, and shared furnishings and physical therapy equipment.

Noroviruses and C. difficile are shed in feces of ill patients as well as those infected asymptomatically (1, 5). A variety of surfaces in LTC facilities can become contaminated with fecal material, leading to environmental transmission by hands of patients, visitors, or nursing staff. Hand washing and environmental cleaning and disinfection procedures are critical elements in infection prevention and control programs in LTC facilities. One difficulty in establishing cleaning and disinfection procedures to prevent environmental transmission of noroviruses or C. difficile is the incomplete guidance for the unique environments of LTC facilities and/or adherence to recommendations when LTC facilities experience diarrheal outbreaks (6, 7). Environmental monitoring with indicators of surface hygiene is a valuable tool for LTC facilities and other healthcare settings, but there are no standard technologies or methodologies used, and many of the available tools are too expensive to implement routinely. Thus, visual inspection is the most common method, which does not correlate well with presence of fecal contamination or surface hygiene (8).

Traditional indicators of fecal contamination, such as fecal coliform bacteria, may not be suitable for indicating the presence of enteric viruses (norovirus) or spore-forming bacteria (C. difficile), which are microorganisms that are more stable on environmental surfaces and have a greater resistance to surface disinfectants than vegetative bacteria. While human noroviruses have been proposed as biomarkers for human fecal contamination, detecting these viruses is inconsistent and often rare, particularly in the absence of an outbreak (8–11). The recently discovered DNA bacteriophage, crAssphage, is a promising tool for detecting human fecal contamination as it is rarely detected in non-human stools and is often present at high concentrations in sewage and human feces without the presence of diarrhea (12–15). In a recent study, crAssphage was used to detect fecal contamination on frequently touched surfaces on cruise ships and on patient hands in LTC facilities experiencing a norovirus outbreak (14). MS2 bacteriophage, a culturable indicator of fecal contamination in environmental waters, is used to model transfer and survival dynamics of viruses on environmental surfaces but is uncommonly detected on environmental surfaces without prior inoculation (16). crAssphage is frequently detected in human feces and on environmental surfaces (12–15), but current methods for detecting crAssphage are PCR-based and cannot assess virus viability.

Portable ATP bioluminescence detection kits have long been used by food processing facilities and are increasingly being used in the healthcare industry for hygienic monitoring to evaluate the efficacy of cleaning procedures (18). ATP drives energetic processes in all living cells, its detection on environmental surfaces indicates the presence of organic material, including microorganisms. ATP test kits are attractive because they can be used onsite for testing surface cleanliness, produce rapid results (within a minute after swabbing) at a relatively low cost. But they cannot be used to evaluate how recently a surface was contaminated with organic material or microorganisms, cellular viability, or the origin of the contamination (such as derived from feces). The primary value of ATP testing is to evaluate the efficacy of cleaning procedures, rather than to evaluate sanitization or disinfection procedures.

We conducted a cross-sectional survey of 11 LTC facilities in South Carolina to evaluate the hygiene of frequently touched surfaces using three monitoring tools; a rapid, portable onsite ATP test system for detecting organic material, the crAssphage indicator of fecal contamination, and human noroviruses (genogroups GI and GII). Our aim was to compare the hygiene of a variety of LTC facility surfaces using different tools and to identify high-touch surfaces and locations in LTC facilities with cleaning deficiencies. Such information could be used by LTC facility directors and environmental service staff to enhance cleaning efficacy and make improvements to infection control procedures.

Methods

LTC facility selection for site visits

This study was approved by the Clemson University and University of Georgia Institutional Review Boards. All 113 long-term care (LTC) facilities identified by the Department of Health and Environmental Control in the midland and upstate regions of South Carolina to have a skilled nursing component were contacted by phone. Facility directors were called a minimum of four times for participation in this study. Eleven of the 113 facilities were recruited, and sampling occurred at these participating sites between January 2016 and March 2016.

Selection of surfaces for hygienic monitoring

Hygienic monitoring was performed at each site by our research teams at the University of Georgia and Clemson University. We consulted with environmental hygiene and nursing staff at each facility to identify and sample at least 30 surfaces that are frequently handled (high-touch surfaces). We performed the sampling in order to reduce variability due to the process of sample collection and to, as much as possible, choose the same categories of surfaces and the same locations within each facility to sample. Categories included handrails, door handles, equipment controls, physical therapy (PT) equipment, door handles (or push bars), TV controls, tables, chairs, nurses’ desks, nursing carts, and janitorial carts. Locations included hallways, bathrooms, patient beds, patient dining rooms, patient lounges, physical therapy rooms, showers, nurses’ desks or carts, and janitorial areas. Our research team grouped sampled surfaces by primary contact persons, or those estimated to be the primary people handling the surfaces, and included patients, visitors, nursing staff, and environmental service staff.

Methods for surface sample collection and analysis

For onsite ATP testing, the Neogen AccuPoint Advanced swab kit (Neogen Food Safety, Michigan, USA) was used following manufacturer’s instructions which included swabbing each surface followed by obtaining the relative light units (RLU) reading from the meter. The technology and default threshold settings for this kit are identical to those of the Neogen AccuPoint Advanced HC kit used in healthcare settings. The same surfaces were immediately swabbed a second time at an adjacent location using macrofoam swabs (Puritan) for detecting noroviruses and crAssphage, as described previously (19). The macrofoam swabs were immediately transferred to a tube containing 50 ml of PBS solution and placed on ice packs for transporting to the laboratory where they were stored at −80°C. For flat surfaces, a 100 cm2 surface area was sampled for each object using a cross hatch sampling pattern and was assisted by a projecting laser device outlining the desired surface area. A comparable surface area was approximated for irregularly shaped surfaces, such as doorknobs, handrails, and equipment controls.

Nucleic acid extraction and molecular detection by realtime qPCR (crAssphage) or multiplex RT-qPCR (norovirus GI and GII and the MS2 internal control) was then performed as described previously (14, 19). MS2 virus added to each sample prior to RNA extraction and used as a control to monitor extraction efficiency and inhibition of the PCR methods (19). Extracted nucleic acid from each sample was tested in duplicate. MS2 RNA was used to monitor inhibition of molecular methods by presence/absence of a positive test (Ct < 35). Samples with RT-qPCR or qPCR results beyond the limit of detection (Ct value >35 for GI norovirus, >37 for GII norovirus (20), and >40 for crAssphage), were assigned the assay lower limit of detection (1.0 log). crAssphage levels in each sample were quantified using a standard curve of extracted crAssphage DNA.

Data Analysis

Qualitative analysis was performed on log transformed crAssphage concentrations and log ATP RLU values obtained from surface samples at each facility. Data were grouped into categories (“high”, “medium”, and “low”), determined by quantiles, with 50% of samples from each facility in the “medium” category and the upper and lower 25% grouped into the “high” and “low” categories, respectively. Odds ratios and 95% confidence intervals were calculated to compare samples having high levels of crAssphage or ATP across categorical variables (surface category, location in LTC facility, and primary contact person). Significance was determined by a Fisher’s exact test with significance described by three levels (p < 0.05, p < 0.01 and p < 0.001). To compare the proportion of samples with high levels of ATP versus those with high levels of crAssphage, a two proportion Z-test for equality of proportions was used with χ2 test of significance at the three defined levels. R (R-project.org) was used for all data analysis including statistics and graphing.

Results

Eleven of the 113 LTC facilities agreed to participate in site visits to conduct our environmental hygiene evaluation; nine were skilled nursing facilities (one of which was also a nursing home), one was a nursing home, and one was a continuing care retirement home. Of the nine facilities that accepted Medicaid, 25–50% of residents were covered by Medicaid in four facilities and greater than 50% of residents were covered by Medicaid in five facilities (Table A.1). The number of beds in each facility ranged from 36 to 220 (median 132 beds) (Table A.1). The capacity of beds filled in each facility at the time of the site visits ranged from 68% to 100% (median 90% capacity) (Table A.1).

Levels of ATP and crAssphage detected in LTC facilities

From the 11 enrolled LTC facilities, at least 30 surfaces (range 30–32) per LTC facility were tested onsite for levels of ATP and for presence and levels of human noroviruses and crAssphage following surface swabbing and laboratory testing. All 337 surfaces for which swab samples were collected tested negative for norovirus. crAssphage was detected on 311 (92.3%) surfaces with concentrations ranging from 1.1 log to 6.2 log genomic copies (median 3.5 log). ATP was detected on 332 (99%) surfaces and ranged from 1.1 log to 5.0 log RLUs (12 to 99,999 RLUs) (median of 3.7 log RLU). Levels of crAssphage and ATP detected on surfaces differed significantly among facilities (Kruskal–Wallis test; p < 0.001 for crAssphage and p < 0.05 for ATP) (Figure A.1). Significant differences were also found when comparing facility characteristics (Medicaid coverage, number of beds and capacity of beds filled at each facility) (Table A.1); however, mean log ATP RLU values and mean crAssphage genomic copy numbers did not increase step-wise with the ordinal variables (Table A.1). One exception was found; levels of crAssphage were significantly greater in the group with a higher capacity of beds filled (Table A.1). However, differences between facilities were strongly significant (accounted for in the two-way ANOVA models) for all crAssphage comparisons, making it difficult to reliably compare facilitiy characteristics (Table A.1).

If the manufacturer suggested threshold values for ATP RLU values (Neogen) were adopted (0–149 pass; 150–299 marginal; above 300 fail), five surfaces would have passed, three would have been considered marginal, and the remaining 324 (98%) would have failed. Because of this and since differences between facilities were found, qualitative scales based on quartiles were created for each facility (Q1 = “low”, Q2 = “medium”, and Q3 = “high”) (Figure A.1). Samples with crAssphage levels below the limit of detection (1.0 log genomic copies) were assigned a value of 1.0 in the quartile calculations. Samples with log genomic copies of crAssphage or log RLU values of ATP within the upper 75th percentile defined for each facility were considered to have “high levels” of crAssphage or ATP, respectively. Defining levels of crAssphage or ATP contamination at each facility allowed us to make comparisons of crAssphage and ATP levels by the variables of type of surface, location, and primary contact person.

LTC facility locations and surfaces with high levels of crAssphage and ATP

Several surfaces and locations within LTC facilities had a greater proportion of samples with high levels of crAssphage or ATP when compared to the others surfaces in the study (Figure 1 A). Using aggregated data from all facilities, handrails and equipment controls were four times as likely to have high levels of crAssphage than other surfaces (odds ratio (OR) 4.1, confidence interval (CI) 2.0–8.5, p < 0.001 for handrails and OR 3.6, CI 1.1–12.8, p < 0.05 for equipment controls) (Figure 1 A). Locations in LTC facilities more likely to have high levels of crAssphage were patient beds (OR 3.9, CI 1.4–12.3, p < 0.05) and hallways (OR 2.6, CI 1.3–5.0, p < 0.01) (Figure 1B). For ATP, the proportion of samples with high levels of ATP did not differ significantly when LTC facility surfaces were compared (p > 0.05 for ORs) (Figure 1A). Only patient dining rooms were more likely than other locations to have high levels of ATP (OR 2.2, CI 1.1–4.2, p < 0.05) (Figure 1B).

Figure 1.

Figure 1.

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Levels of crAssphage and ATP detected on LTC facility surfaces (A) and locations (B). The proportion of samples with high levels of crAssphage are shown in red. The proportion of samples with high levels of ATP are shown with circular markers. High levels of crAssphage and ATP were defined for each LTC facility and refer to samples with log genomic copies of crAssphage or log RLU values of ATP within the upper 75th percentile.

Aggregating data across facilities allowed statistical comparison of the LTC facility surfaces and locations most often having high levels of crAssphage. However, trends in the proportion of samples with high levels of crAssphage were observed for unique combinations of surfaces and their location within LTC facilities (Figure 2). Handrails and equipment controls on patient beds had at least 50% of samples with high levels of crAssphage and/or ATP. In hallways, handrails and door handles had at least 50% of samples with high levels of crAssphage or ATP. Other combinations with at least 50% of samples having high levels of crAssphage or ATP included chairs in patient lounges and desks at nurses’ stations.

Figure 2:

Figure 2:

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Heatmap for the percent of samples with high levels of crAssphage or ATP on combinations of surface and location within LTC facilities. High levels of crAssphage and ATP were defined for each LTC facility and refer to samples with log genomic copies of crAssphage or log RLU values of ATP within the upper 75th percentile.

Levels of crAssphage and ATP on surfaces by primary contact person

LTC facility surfaces were also categorized by primary contact person, or groups of people (i.e. nurses, environmental service staff, patients, or patients and visitors) most likely to contact the surfaces. This was done to investigate whether or not a particular group (such as patients, for example) disproportionally contributed to higher levels of contamination in the facilities. For crAssphage, there were no differences due to primary contact person for proportions of samples with high levels of crAssphage (OR with p > 0.05). However, surfaces touched by patients and visitors were twice as likely to have high levels of ATP compared to those touched by primarily by nursing and janitorial staff or by patients alone (OR 1.8, CI 1.1–2.9, p < 0.05). Some trends among the combinations of surfaces and the primary contact persons for that surface were observed (Figure 3). Among surfaces touched primarily by patients and visitors, those with > 50% of samples with high levels of crAssphage or ATP included handrails and chairs. Handrails touched primarily by patients (patient bed handrails) had at least 50% of samples with high levels of crAssphage and ATP. Equipment controls primarily contacted by nurses and the side of nurses’ desks primarily touched by nurses had at least 50% of samples with high levels of crAssphage or ATP.

Figure 3:

Figure 3:

Open in a new tab

Heatmap for the percent of samples with high levels of crAssphage or ATP on combinations of surface and primary contact person group within LTC facilities. High levels of crAssphage and ATP were defined for each LTC facility and refer to samples with log genomic copies of crAssphage or log RLU values of ATP within the upper 75th percentile.

crAssphage and ATP comparisons among surfaces, locations and primary contact persons

When comparing the proportion of surfaces with high levels of crAssphage to those with high levels of ATP, apart from handrail and equipment control samples, no significant differences were found (p > 0.05) (Table A.2). Similarly, only patient dining rooms differed significantly when the proportion of samples with high levels of crAssphage were compared to those with high levels of ATP (p < 0.001) (Table A.2). No group yielded statistically significant differences between levels of crAssphage and levels of ATP (p > 0.05) by primary contact person (Table A.2). Looking at trends for surface and location combinations, however, patient bed handrails had over 50% of samples with high levels of both ATP and crAssphage (Figure 2). Between 25–50% of samples taken from patient lounges and those taken from PT equipment had high levels of ATP and crAssphage (Figure 2).

Discussion

Infection control programs in LTC facilities should include rigorous cleaning and disinfection procedures for high-contact surfaces as contaminated surfaces contribute significantly to transmission of noroviruses and C. difficile in healthcare settings (17, 21–23). We used ATP and crAssphage to evaluate the hygiene of high-touch environmental surfaces and locations in 11 LTC facilities. Despite high positivity rates for crAssphage and ATP detected, we identified specific surfaces and locations within LTC facilities contaminated with the highest levels of organic debris and/or evidence of fecal contamination.

Surfaces and locations in LTC facilities with high levels of crAssphage or ATP were similar to those found in other studies on cruise ships, which share similarities to LTC facilities in that the cabins are home-like environments and there is congregation in common areas, and in healthcare settings, which have much of the same types of patient care equipment as LTC facilities. For instance, on cruise ships experiencing a recent norovirus outbreak, surfaces with the highest levels of crAssphage (>3.5 log genomic copies) included handrails in atriums, arm rests on wheelchairs, TV remote controls, and toilet seats (14). High-touch surfaces in healthcare settings with ATP RLU values above 1000 (3.0 log) included bathroom sinks, handrails on beds and in bathrooms, overbed tables, TV remote controls, computer keyboards, and nurses’ desks (24–31). However, the proportion of surfaces with high levels of crAssphage or ATP contamination were greater in our study than in others. For instance, one study similarly found 86–100% of high-touch surfaces in hospitals had failing ATP scores (with a 500 RLU failure threshold) (26), but the range was typically lower among other studies (14% to 61% in healthcare settings) (24, 27–31). On cruise ships experiencing a recent norovirus outbreak 52% of high touch surfaces collecting during the outbreak and 39% of samples collected 3 weeks later had high levels of crAssphage (14).

The reason for this is unclear, except possibly the few number of studies for which to compare. As of April 2021, there were only two studies using ATP for environmental monitoring in LTC facilities (32, 33), despite substantial growth in the number of studies using ATP for evaluating cleaning practices in other healthcare settings over the last decade (8, 18, 34). Similarly, only the single study on cruise ships used crAssphage as an indicator of fecal contamination on environmental surfaces, despite its increasing use in assessing fecal contamination of water (13, 14). ATP failure thresholds and raw RLU values were not reported in one of the LTC facility studies, but the authors correlated ATP levels with bacterial counts and found 58% of high-touch surfaces had ATP levels above background levels (32). In the other study, which included three LTC facilities, ATP RLU values were lower than found our study (they did not exceed 250 RLUs per surface), but personal communication with the authors indicated that, unlike in our study, the surfaces were cleaned immediately before ATP testing (33). It is possible that if more studies in LTC facilities are performed, higher rates of ATP failure and crAssphage detection could be reported, suggesting a modified benchmark might be warranted. Failure thresholds have been modified from manufacturer default settings depending on limits appropriate for the industry, facility or location therein, correlation with microbial indicators of hygiene, or what can be achieved following best cleaning practices (8, 18, 24–29). A modified benchmark might particularly be needed due to the home-like atmosphere of LTC facilities and perhaps also due to the higher frequency and duration of time for patient visitation, potentially leading to higher levels of contamination in common areas.

Studies monitoring fecal contamination in healthcare settings are limited; the majority of which detect fecal pathogens, often following outbreaks (17, 23, 35, 36). In our study, noroviruses were not detected, supporting previous literature that they and other enteric pathogens are rarely detected unless there is a current or recent outbreak (8–11). However, we cannot rule out the possibility that noroviruses were present but not detected as the limit of detection for the macrofoam swab method was 3.4 log for noroviruses. Detecting crAssphage DNA indicates fecal contamination but cannot determine how recent the contamination occurred or viral infectivity. Non-infective viral genomic material can persist on surfaces from days to months, even following surface disinfection (17). ATP methods are attractive as they are less expensive than methods requiring laboratory testing and produce near realtime results. However, ATP is found in all living cells (i.e. human, those in food debris, and bacterial) and can persist on environmental surfaces for days to weeks (37); as such, ATP indicates presence of organic debris that is not necessarily microbial and contamination that is not necessarily recent. Some studies report correlation between detecting ATP and viable bacteria, but it is generally not considered a reliable indicator of microbial or fecal contamination (18). In one study, levels of MS2 bacteriophage, a fecal indicator virus, and ATP in the workplace were significantly reduced after cleaning surfaces and hands; although, a direct correlation was not found (16). ATP testing has the most value when it is used to evaluate how well a surface is cleaned or to quantify improvements in cleaning practices over time (18). Audit and feedback systems using ATP have enhanced the efficacy of cleaning high-touch surfaces in healthcare settings and their implementation has been associated with reduced numbers of healthcare associated infections in hospitals (25, 33, 38). Applying audit and feedback systems to locate surfaces where fecal contamination was not adequately removed after cleaning, such as using the crAssphage indicator, might more specifically identify locations where noroviruses and C. difficile persist after cleaning.

This study has several limitations and drawbacks to the study design. Primarily, levels of ATP do not correlate with microbial contamination and the association between detecting crAssphage DNA versus viable enteric pathogens is not established. Given the high rate of crAssphage detection in this study, it unlikely that crAssphage presence is indicative of risk for diarrheal disease transmission or outbreaks. Although currently undefined, future studies in outbreak settings might quantify risk associated with levels of crAssphage surface contamination exceeding a certain threshold. Next, we did not compare the characteristics of the 11 South Carolina LTC facilities included in our study with the 102 facilities in the state that did not participate; therefore, extrapolation of our findings beyond the facilities in our study was not possible. In the study design, we attempted to sample the same number and types of surfaces in each facility. We did not, however, control for how recently a person contacted the surfaces or how recently the surfaces were cleaned. In addition, sites were visited at one time point and we did not provide direct feedback to the LTC facility directors and staff participating in this study. Ideally, monitoring would be performed on a routine basis and a system of audit and feedback would be established. Facility staff could then identify where there are cleaning deficiencies and apply corrective actions or educational interventions when necessary.

Conclusions

Nearly all high-touch surfaces in the LTC facilities of this study were contaminated with the crAssphage indicator of fecal contamination and organic material resulting in failing ATP cleanliness scores. Noroviruses were not detected on environmental surfaces at any facility. Using a qualitative scale accounting for differences between the facilities, we identified surfaces and locations having the highest levels of ATP and/or crAssphage. Combining crAssphage and ATP monitoring in a longitudinal audit and feedback program could help LTC facility staff identify surfaces where organic material and/or fecal contamination persists after cleaning; this is particularly the case if threshold values associated with risk of transmission or outbreaks of diarrheal disease are established. Such information is intended to enhance the prevention and control of noroviruses and C. difficile in LTC facilities.

Supplementary Material

1

Acknowledgments

We thank tremendously the technical support provided by Alison Payton (Center for Food Safety, UGA) and M. Anuradhi Prabamini Makawita (Clemson University) for her vital contributions in the review of literature.

Funding

Research on hygienic monitoring in LTC facilities was funded in part by Agriculture and Food Research Initiative competitive grant 2011-68003-30395 from the USDA National Institute of Food and Agriculture and grant 5R01HS025987-03 and Agency for Healthcare Research and Quality competitive grant R01 HS025987 from the National Institutes of Health.

Footnotes

Conflicts of interest

There are no conflicts of interests.

Disclaimer

The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

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