Abstract
Background
Adenosine triphosphate (ATP)-based monitoring systems can detect the amount of organic matter that remains on hospital surfaces after cleaning. We evaluated an ATP-based monitoring system in assessing contamination of high touched objects in rooms occupied by patients on methicillin resistant S. aureus precautions.
Methods
We compared the ATP to standard aerobic cultures as well as to gloved hand culture to predict risk of healthcare-worker hand contamination.
Results
More than a third of high touch object surfaces were measured unclean with ATP yet only reflects about 5% chance of contaminating healthcare-workers’ hands.
Conclusions
Our study emphasizes the shortcomings of using the ATP system even in pathogen specific environment such as surfaces in methicillin resistant S. aureus rooms.
Keywords: Environment, Healthcare-associated infections, Hand hygiene, Infection prevention, Infection control, MRSA
1. Introduction
The Centers for Disease Control and Prevention have recommended that hospitals ensure compliance by housekeeping staff with cleaning and disinfecting procedures [1]. They recommend a structured education of environmental management service staff, including baseline evaluation of thoroughness of cleaning, evaluation of competency, and a need for regular monitoring of the program to be performed and documented by health care facilities. A monitoring system available involves the detection of adenosine triphosphate (ATP), a compound used in the metabolic processes of cells on the surface. Its detection on environmental surfaces at clinics and hospitals has been used to assess the adequacy of routine cleaning procedures [2]. However, variability in readings was demonstrated in vitro among different drug-resistant pathogens along with methicillin-resistant Staphylococcus aureus (MRSA) exhibiting the highest bioluminescence readings [3]. We evaluated an ATP-based monitoring system in assessing contamination of high touched objects (HTOs) in rooms occupied by patients on MRSA precautions. We compared it to standard aerobic cultures as well as to gloved hand culture for MRSA to predict the risk of healthcare-worker (HCW) hand contamination from surfaces in these rooms. The ATP assay is used to measure the effectiveness of environmental cleaning. In this study, we evaluated its use in rooms occupied by patients in MRSA isolation and how contamination of the environment can translate to hand contamination that is considered the most common way of transmission from environment to another patient.
2. Materials and Methods
This study was conducted in the single-site inpatient facility at the Fargo Veteran Affairs Healthcare System (VAHCS). The Fargo VAHCS is a joint accredited mixed medical and surgical hospital with 71 inpatient beds in the US Upper Midwest. We conducted a 4-month prospective survey of a convenient sample of HTOs in MRSA contact precaution inpatient rooms after terminal cleaning. Routine terminal cleaning was defined as the cleaning of patient rooms after the patient was discharged in a systematic manner (moving from low-touch surfaces to HTOs) with a fresh cleaning cloth soaked in an EPA-approved hospital-grade germicide environmental cleaning solution (CaviCide Disinfectant and Cleaner (quaternary ammonium and 17% alcohol), by Metrex, Orange, CA). In each location, the ATP surface sample swab (3M CleantraceTM with UXL100 swabs, St Paul, MN) was used on 16 cm [2] surface of 5 HTOs after terminal cleaning. HTOs included phone, call button, bed rail, toilet rail, over the bed table, and/or remote control depending on location. After the sample is collected, it is exposed to lysis buffer (an ATP-releasing agent) and luciferin and luciferase (ATP-activated light-producing enzymes) [2]. The amount of ATP present can then be recorded by the amount of light emitted during the enzymatic reaction (denoted as relative light units or RLUs). Another adjacent 16 cm2 area of the HTO was sampled with premoistened culture swabs on each surface. Culture swabs were then directly inoculated on to blood agar and incubated at 37 °C for 48 hours, and aerobic colony counts were counted (denotes as Aerobic colony count or ACC). In a similar fashion, investigators donned sterile gloves for a third adjacent surface area and had a contact of 5 seconds with each surface before imprinting on MRSA selective media to simulate hand contamination after contact. Surfaces with less than 2.5 colony forming units (CFU)/cm2 on ACC, less than 100 RLUs based on the ATP system, and no MRSA growth on MRSA selective media were considered as clean.
Pearson χ2 was applied to compare the proportions of surfaces classified clean based on the different methods. Sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of ATP system were calculated relative to aerobic culture and risk of hand contamination. All analyses were conducted utilizing SPSS statistical software (version 19 for Windows, IBM, Armonk, NY). Data was deemed significant at p < 0.05.
3. Results
A total of 225 HTOs were sampled from 45 inpatient rooms that had current MRSA contact precautions. Based on ATP assay, 88 (39.1%) of the HTO surfaces had RLUs > 100 (range 104–1180) and were not considered as clean. Total surfaces with more than 2.5 CFU/cm2 on ACC were 77 (34.4%) while only 11 (4.9%) were positive for MRSA growth on MRSA selective-media (range of ACC was 3–90 and average MRSA CFU on the MRSA positive sites was 9). Of these HTOs that were positive for MRSA growth, there was a wide range of corresponding RLU levels from 8 to 631 with a mean of 170 RLUs compared to 5–3599 RLU (mean of 173 RLU) for non-MRSA contaminated surfaces. The most common HTOs to show contamination across testing methods were the bedrail, over the bed table, and the phone.
Sensitivity, specificity, PPVand NPV of ATP system was measured relative to ACC and MRSA hand contamination. Sensitivity, specificity, PPV, and NPV of ATP system were 52%, 13%, 45%, and 90% respectively when measured against aerobic culture. Relative to the risk of hand contamination, sensitivity, specificity, PPV, and NPV were 55%, 19%, 7%, and 99%, respectively. The low PPV and high NPV were evidence of the low number of positive MRSA growth from hand printing relative to the number of surfaces with more than 100 RLUs on ATP. There is no significant correlation between ATP based assay and ACC with Pearson's correlation coefficient of 0.16, p = 0.28 (Table 1). Similarly, when ATP was compared to risk of hand contamination, correlation coefficient was also not significant at 0.05, p = 0.74 (Table 1).
Table 1.
Pearson Correlations between ATP surface sampling, culture swabs plated on blood agar, and imprinting on MRSA selective media.
| MRSA | Blood agar | ATP | ||
|---|---|---|---|---|
| MRSA | Pearson Correlation | 1 | −0.147 | −0.051 |
| Sig. (2-tailed) | 45 | 0.337 | 0.738 | |
| N | 45 | 45 | ||
| Blood Agar | Pearson Correlation | −0.147 | 1 | 0.164 |
| Sig. (2-tailed) | 0.337 | 45 | 0.280 | |
| N | 45 | 45 | ||
| ATP | Pearson Correlation | −0.051 | 0.164 | 1 |
| Sig. (2-tailed) | 0.738 | 0.280 | 45 | |
| N | 45 | 45 |
MRSA, methicillin resistant S. aureus; ATP, adenosine triphosphate (ATP)-based monitoring system.
ATP surface samples were derived from 3MTM CleantraceTM with UXL100 swabs, St Paul, MN.
4. Discussion
There is a significant role that the environment plays in the transmission of healthcare associated pathogens. Patients infected or colonized with pathogens such as MRSA, Clostridioides difficile, vancomycin-resistant Enterococci (VRE), and resistant gram-negative organisms frequently contaminate their surroundings which can potentially contribute to transmission of pathogens by serving as a source from which HCWs contaminate their hands or gloves [4], [5], [6]. To protect Veterans from direct or indirect spread of these pathogens, the Centers for Disease Control and Prevention and the VAHCS recommend contact precautions for patients colonized or infected with MRSA [7]. Additionally, compliance and monitoring of housekeeping staff is recommended [1]. We evaluated the performance of an ATP-based monitoring system against aerobic bacterial cultures and correlated with risk of hand contamination of MRSA in rooms previously occupied by an MRSA patient.
We found that in our institution, 39.1% of HTOs were deemed not clean based on ATP assay and 34.4% based on aerobic cultures despite terminal cleaning. This translates to a 4.9% chance of contaminating the gloved hand with MRSA. This simulates HCWs’ hands, which is a known risk in the transmission of drug resistant pathogens
Relative to ACC and MRSA hand contamination risk, the ATP assay performed poorly with no significant correlations and low sensitivities, specificities and positive predictive values but does have a decent negative predictive value. This means an environmental surface deemed clean by an ATP assay is likely to have low bacterial burden and subsequently has low risk for MRSA hand contamination. Therefore, the ATP assay can be considered a conservative approach in assessing the cleanliness of surfaces in patients’ rooms. However, the low sensitivities, specificities and positive predictive values of ATP assay may lead to enhanced cleaning of uncontaminated surfaces which may not necessarily be viewed as a negative consequence. These results were not unexpected as have been reported by Boyce et al., Aycicek et al., and Shama and Malik [6,8,9]. There are many factors that influence ATP readings. Intrinsically, ATP detects organic material on surfaces but do not discriminate viable aerobic organisms unlike aerobic cultures. Additionally, different pathogens exhibit different RLU readings. In a study of different types of bacteria, MRSA had the highest ATP readings followed by Pseudomonas aeruginosa and VRE [3]. We speculated that the higher inherent RLU readings for MRSA would increase ATP correlation to the aerobic culture method if we targeted MRSA rooms. However, the fact that these readings come from rooms with current MRSA contact precautions does not equate MRSA as the sole contributor to the environmental ATP. Contaminants other than bacteria may also interfere with RLU readings such as the cleaning cloth, disinfectants, any organic substrate, or even the material of surfaces being cleaned [6].
Another limitation of ATP is the lack of standardized threshold for what would be classified as clean. We utilized 100 RLU benchmark as it offered the closest correlation with aerobic culture levels of <2.5 CFU/cm2 as determined by Mulvey et al. [10]. However, different studies have used different benchmark values. Also, different studies utilized various bioluminometers or ATP devices which may have different recommended cutoff values. Despite these limitations, many institutions still use the ATP system for monitoring of hospital cleaning. This may be due to its relatively ease of use and the potential for real time feedback of housekeeping staff. Also, the high negative predictive value allows the determination that a surface is clean.
Our study illustrates the shortcomings of the use of the ATP system even in pathogen specific environment such as surfaces in MRSA rooms. More than a third of these surfaces are measured unclean with ATP and reflects about 5% chance of contaminating HCWs’ hands.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author contributions
AM, KM, DG, and TL all contributed to the study design. AM and DG contributed to the statistical analysis. KM and TL monitored and performed the sample collection.
Acknowledgements
These findings are the result of work supported with resources and use of facilities at the Fargo Veterans... Affairs Health Care System. The contents do not represent the views of the US Department of Veterans... Affairs.
Declaration of competing interest
There was no financial support to declare for this study. The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Data available statement
No data, models, or code were generated or used during the study.
Ethics statement
Ethics approval were waived for this study because no patients' data were reported.
Informed consent
Infromed consent was waived for this study because no patients' data were reported.
References
- 1.Guh A., Carling P. Options for evaluating environmental cleaning’ Division of Healthcare Quality Promotion (DHQP) Center Dis. Control Prevent. (CDC) 2010;102(2) Available at: Options for Evaluating Environmental Cleaning | HAI | CDC (Accessed: 25 January 2020. [Google Scholar]
- 2.Luick L., Thompson P.A., Loock M.H., et al. Diagnostic assessment of different environmental cleaning monitoring methods. Am. J. Infect. Control. 2013;41(8):751–752. doi: 10.1016/j.ajic.2012.09.019. [DOI] [PubMed] [Google Scholar]
- 3.Heller M., Thompson P.A., Loock M.H., et al. Variability of adenosine triphosphate-based bioluminescence assay readings among drug-resistant pathogens. Infect. Control Hosp. Epidemiol. 2012;33(12):1286–1288. doi: 10.1086/668444. [DOI] [PubMed] [Google Scholar]
- 4.Klevens R., Edwards J., Richards C.L., Jr, et al. Estimating health care-associated infections and deaths in U.S. hospitals. Publ. Health Rep. 2007;122(2):160–166. doi: 10.1177/003335490712200205. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Boucher H., Corey G. Epidemiology of methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis. 2009;46(5):344–349. doi: 10.1086/533590. [DOI] [PubMed] [Google Scholar]
- 6.Boyce J.M., Havill N.L., Dumigan D.G., et al. Monitoring the effectiveness of hospital cleaning practices by use of adenosine triphosphate bioluminescence assay. Infect. Control Hosp. Epidemiol. 2015;30:678–684. doi: 10.1086/598243. [DOI] [PubMed] [Google Scholar]
- 7.Vol. 11301. Veterans Health Administration (VHA); Washington, DC: 2017. pp. 7–10.https://www.va.gov/vhapublications/ViewPublication.asp?pub_ID=5616 (Management of Infectious Diseases and Infection Prevention and Control Programs). DirectiveAvailable at. Accessed 18 February 2020. [Google Scholar]
- 8.Aycicek H., Oguz U., Karci K. Comparison of results of ATP bioluminescence and traditional hygiene swabbing methods for the determination of surface cleanliness at a hospital kitchen. Int. J. Hygiene Environ. Health. 2006;209:203–206. doi: 10.1016/j.ijheh.2005.09.007. [DOI] [PubMed] [Google Scholar]
- 9.Shama G., Malik D.J. ‘The uses and abuses of rapid bioluminescence-based ATP assays. Int. J. Hygiene Environ. Health. 2013;216:115–125. doi: 10.1016/j.ijheh.2012.03.009. [DOI] [PubMed] [Google Scholar]
- 10.Mulvey D., Redding P., Robertson C., et al. Finding a benchmark for monitoring hospital cleanliness. J. Hosp. Infect. 2011;77(1):25–30. doi: 10.1016/j.jhin.2010.08.006. [DOI] [PubMed] [Google Scholar]