Highlights
- •Visual inspection had the highest clean rate and the lowest pass rate by adenosine triphosphate (ATP)
- •No correlation between visual inspection and ATP interpretation
- •Weak positive correlation between performance observation and ATP interpretation
- •Results of visual inspection, performance observation and ATP were not consistent
Abstract
Background
Environmental cleaning is an effective measure to prevent infections. However, performance observation has been rarely delineated. This study aimed to compare correlations among visual inspection, performance observation, and effectiveness by using adenosine triphosphate bioluminescence (ATP bioluminescence) as a comparator to find out which method is better to assess hospital cleanliness.
Methods
This prospective study was conducted at a medical center from April 2019 to October 2020. Seven high-touch surfaces were evaluated during and after terminal cleaning by performance observation, visual inspection, and ATP bioluminescence.
Results
The scores by performance observation, visual inspection, and ATP were 55.4%, 87.5%, and 26.6% after cleaning. The correlations between performance observation and visual inspection and between performance observation and ATP interpretation were weak positive (φ = 0.300, 0.324, P < .001). No correlation was between the visual inspection and ATP interpretation (φ=0.137). The median of ATP readings was lower in “compliant” group by performance observation and “clean” group by visual inspection than “not compliant” group and “not clean” group (P < .001).
Conclusions
Performance observation combined with ATP would be preferred to include to audit cleanliness on high-risk surfaces. Visual inspection would be a rapid and time-saving assessment tool on low-risk surfaces.
Key Words
Background
Infections with multidrug-resistant organisms have become a critical issue across the world because of increased morbidity, mortality, and the financial burden of health care. The surfaces surrounding patients are usually contaminated by multidrug-resistant organisms and thereby increase the pressure of colonization and risk of infection.
1
Researches proved that healthcare associated infections were prevented by enhanced environmental cleaning. In Watson, Knelson and Li et al's studies, the infection rates of vancomycin-resistant Enterococcus, methicillin-resistant Staphylococcus aureus and multidrug-resistant Acinetobacter baumannii decreased by 50%, 96%, and 62% after enforcement of environmental cleaning, respectively.2
, 3
, - Knelson L.P.
- Williams D.A.
- Gergen M.F.
- Rutala W.A.
- Weber D.J.
- Sexton D.J.
A comparison of environmental contamination by patients infected or colonized with methicillin-resistant Staphylococcus aureus or vancomycin-resistant Enterococci:a multicenter study.
Infect Control Hosp Epidemiol. 2014; 35: 872-875
4
In a multicentre study involved 11 acute care hospitals found that vancomycin-resistant enterococci infections decreased by 37% by introducing cleaning bundle.5
Furthermore, according a system review, enhanced cleaning, and decontamination showed significant reductions in Clostridioides difficile infection.6
There are several methods to evaluate the effectiveness of cleaning in hospital environment, including direct practice observation (performance observation), swab cultures, agar slide cultures, fluorescent markers, adenosine triphosphate bioluminescence (ATP bioluminescence), and visual inspection.
7
, Guh A., Carling P., Options for evaluating environmental cleaning. Available at: https://www.cdc.gov/hai/pdfs/toolkits/Environ-Cleaning-Eval-Toolkit12-2-2010.pdf. Accessed June 9, 2021.
8
ATP bioluminescence measures adenosine triphosphate (ATP) found in all animal, plant, bacterial, yeast, and mold cells. The luminometer measures generated light and reports results in relative light units (RLU). The higher the RLU number, the more ATP present, and the dirtier the surface.9
Hygiena. UltraSnap surface ATP Test. Available at: file:///C:/Users/Vgh00/Downloads/INS0039%20-%20UltraSnap_RevC_All%20Languages.pdf. Accessed December 20, 2020.
Though audit and feedback by visual inspection is easy to implement and no devices are needed, visual inspection showed significantly different in results compared with the ATP bioluminescence and microbiologic sampling (aerobic colony counts). Microbial load cannot be visible so that the environmental cleanliness is usually overestimated when using visual inspection.
10
, 11
, 12
Compared with aerobic colony counts, ATP bioluminescence showed significantly different or poor and/or moderate correlation.12
, 13
Fluorescent marker method had the lowest clean rate compared with visual inspection, ATP bioluminescence, and microbiologic sampling.14
, 15
Housekeepers are expected to follow the standard of procedures to clean patient rooms, so it is essential to make sure that they do wipe to remove contaminants and disinfect the surfaces. However, the comparison of results between performance observation and ATP is rare. This study aimed to compare correlation between visual inspection and performance observations and effectiveness by using ATP bioluminescence test as a comparator in order to find out which method would be better to assess hospital cleanliness.
Materials and methods
Design and setting
We performed a prospective study which was conducted in a 17-bed adult medical intensive care unit with approximately 352 annually admissions at a tertiary hospital in Taiwan from April 2019 to October 2020. Cleaning performance observation was performed according to the environmental checklist for monitoring terminal cleaning released by Centers for Disease Control and Prevention in 2014 to select sampling areas of high-touch surfaces in patient rooms, including bed controls, bed rails, cart pulls, light switches, machine controls, tray tables, and call buttons.
16
Centers for Disease Control and Prevention. CDC environmental checklist for monitoring terminal cleaning. Available at: https://www.cdc.gov/hai/pdfs/toolkits/Environmental-Cleaning-Checklist-10-6-2010.pdf. Accessed December 20, 2020.
Data collection
The housekeepers started to do terminal cleaning after patients were transferred or discharged, the researcher also started to observe directly the practices of cleaning at the same time and recorded “compliant” or “not compliant” when surfaces were cleaned and disinfected properly or on the contrary.
16
The high-touch surfaces were disinfected with solution which contained Sodium dichloroisocyanurate (NaDCC). Right after the surfaces were cleaned, the researcher inspected the surfaces and recorded “clean” or “not clean” when surfaces were free of dust, debris, and stains immediately after terminal cleaning or on the contrary.Centers for Disease Control and Prevention. CDC environmental checklist for monitoring terminal cleaning. Available at: https://www.cdc.gov/hai/pdfs/toolkits/Environmental-Cleaning-Checklist-10-6-2010.pdf. Accessed December 20, 2020.
17
Ten minutes after surfaces were cleaned and disinfected, Hygiena Ultrasnap Surface ATP test was applied to swab a standard 10 × 10 cm area on selected surfaces defined by a sampling template. The sampling template was disinfected with 75% alcohol pads to dry for at least 2 minutes before and after sampling. Then, the sampling template was directly put on the selected surfaces without any position adjustment to minimized touching the sampling area and the residual effect of alcohol. After completing sampling, swabs were replaced back in swab tube and all liquid in bulbs was expelled to activate the reaction. After shaking for 5-10 seconds, the entire UltraSnap device was inserted into Hygiena luminometer (SystemSURE Plus). Once activated, sample must be read within 30 seconds. We followed instructions by the kit manufacturer. Hygiena luminometers less than 10 RLU (relative light unit, RLU) was interpreted as “pass,” indicating that surface was considered clean.
9
The designated cleaner and the researcher were assigned to clean high-touch room surfaces and to be in charge of evaluating and sampling, respectively.Hygiena. UltraSnap surface ATP Test. Available at: file:///C:/Users/Vgh00/Downloads/INS0039%20-%20UltraSnap_RevC_All%20Languages.pdf. Accessed December 20, 2020.
Statistical analysis
Descriptive statistics were calculated including numbers, percentage, mean, standard deviation, median, and interquartile range. Inferential statistics were analyzed with SPSS (version 22) to determine correlation between results of performance observation, visual inspection and ATP interpretation by using χ²test or Fisher's exact test. The phi coefficients were calculated to measure strength between 2 sets of data. The phi coefficient refers to the meaning of Pearson's Correlation coefficients, values 0.01-0.19 as no or negligible, 0.2-0.39 as weak positive, 0.4-0.69 as medium positive, 0.7-1.0 as strong positive.
18
The ATP readings were compared between “not compliant” and “compliant,” and between “not clean” and “clean” respectively by using Mann-Whitney U test.SAGE Research Methods Datasets. Learn to use the phi coefficient measure and test in R with data from the welsh health survey. Available at: https://methods.sagepub.com/base/download/DatasetStudentGuide/phi-coefficient-whs-2009-r. Accessed December 20, 2020.
The institutional review board of the hospital approved the study protocol (CW18285B) and the study protocol was registered in the trial register (registration number NCT03908398).
Results
The total of 504 samples were collected. The “clean” rate by visual inspection was 87.5%. The “compliant” rate by performance observation was 55.4%. The “pass” rate by ATP interpretation was 26.6%. The phi coefficient was 0.300 between the results of visual inspection and performance observation (P < .001). The phi coefficient was 0.137 between the results of visual inspection and ATP interpretation (P < .005). The phi coefficient was 0.324 between the results of performance observation and ATP interpretation (P < .001). The “clean” rate was the highest and the “pass” rate was the lowest among the 3 methods. While the correlations were weak positive between visual inspection and performance observation and between performance observation and ATP interpretation, there was no correlation between visual inspection, and ATP interpretation (Table 1).
Table 1Correlation between visual inspection, performance observation, and ATP interpretation.
| “Clean” rates byvisual | “Compliant” rates by performance | “Pass” rates by ATP interpretation | P(φ)(Visual vs performance) | P(φ) (Visual vs ATP interpretation) | P(φ) (Performance vs ATP interpretation) | ||||
|---|---|---|---|---|---|---|---|---|---|
| Bed control | 52 (100.0%) | 35 (67.3%) | 15 (28.8%) | − (−) | -(-) | .011(.353) | |||
| Bed rail | 101 (97.1%) | 61 (58.7%) | 38 (36.5%) | .068 (.205) | .298(.131) | .000(.394) | |||
| Cart pull | 93 (95.9%) | 63 (64.9%) | 28 (28.9%) | .013(.282) | 1.000(.018) | .024(.230) | |||
| Light switch | 123 (87.2%) | 73 (51.8%) | 30 (21.3%) | .000(.311) | .121(.147) | .000(.398) | |||
| Machine control | 36 (56.3%) | 27 (42.2%) | 13 (20.3%) | .003(.371) | .021(.289) | .001(.434) | |||
| Tray table | 21 (70.0%) | 15 (50.0%) | 6 (20.0%) | .109(.364) | .029(.429) | .014(.509) | |||
| Call button | 15 (93.8%) | 5 (31.3%) | 4 (25.0%) | 1.000(.174) | 1.000(.149) | .003(.856) | |||
| Total | 441 (87.5%) | 279 (55.4%) | 134 (26.6%) | .000(.300) | .002(.137) | .000(.324) | |||
ATP interpretationl, ATP readings less than 10 RLU (relative light unit, RLU) were interpreted “pass” :ATP readings more than 10 RLU (relative light unit, RLU) were interpreted “not pass”.
† Fisher exact test.
‡ x2 test.
Among these high-touch surfaces in patient rooms, bed controls, bed rails and cart pull had “clean” rates more than 95%. However, the highest “compliant” rate was 67.3% for bed controls and the highest “pass” rate was only 36.5% for bed rails. Machine controls had the lowest “clean” rate 56.3%, Call buttons had the lowest “compliant” rate 31.3% and Tray tables had the lowest “pass” rate 20.0%. Most surfaces had no correlation or weak positive correlations between the results of any 2 methods except tray tables with medium positive correlation between visual inspection and ATP interpretation (φ = 0.429), machine controls and tray tables with medium positive correlation between performance observation and ATP interpretation (φ = 0.434, 0.509), call buttons with strong positive correlation between performance observation and ATP interpretation (φ = 0.856) (Table 1).
The mean, median and the interquartile range of ATP readings for 504 samples were 138.39, 33.00, and 86.75 RLU. The most contaminated item was machine controls with the highest mean 297.92, median 73.00 and interquartile range 246; the least contaminated item was cart pulls with the lowest mean 54.25, median 20.00 and interquartile range 42. All means were much higher than medians indicated diverse contaminant levels among surfaces (Table 2).
Table 2ATP readings (RLU) for selected surfaces.
| Mean (SD) | Median | Interquartile range(IQR) | |||
|---|---|---|---|---|---|
| Bed control | 87.50 (218.94) | 25.50 | 56.25 (6.50-62.75) | ||
| Bed rail | 96.72 (402.08) | 24.00 | 56.00 (7.00-63.00) | ||
| Cart pull | 54.25 (191.60) | 20.00 | 41.50 (8.50-50.00) | ||
| Light switch | 166.93 (266.69) | 45.00 | 179.00 (13.00-192.00) | ||
| Machine control | 297.92 (884.73) | 73.00 | 246.00 (17.00-263.00) | ||
| Tray table | 203.63 (534.20) | 33.50 | 122.75 (9.75-132.50) | ||
| Call button | 72.81 (94.67) | 44.50 | 76.00 (9.25-85.25) | ||
| Total | 138.39 (430.55) | 33.00 | 86.75 (9.00-95.75) | ||
The median of ATP readings by performance observation were 79.00 RLU for “not compliant” group and 14.00 RLU for “compliant” group (P < .001), indicating that there was significant difference between the 2 groups of data. All high-touch surfaces but bed controls had significantly lower ATP readings in “compliant” group than “not compliant” group. The median of ATP readings by visual inspection were 158.00 RLU for “not clean” group and 26.00 RLU for “clean” group (P < .001), indicating that there was significant difference between the 2 groups of data. Among these high-touch surfaces in patient rooms, bed rails, light switches, machine controls and tray tables also had significantly lower ATP readings in “clean” group than “not clean” group. The results showed that the surfaces which were cleaned and disinfected properly and free of dust, debris, and stains were cleaner than the opposite (Table 3).
Table 3Comparing ATP readings (RLU) between “compliant” and “not compliant” by performance observation and between “clean” and “not clean” by visual inspection.
| ATP readings (RLU) for performance observation | ATP readings (RLU) for visual inspection | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Not compliant, median (IQR) | Compliant, median (IQR) | P | Not clean, median (IQR) | Clean, median (IQR) | P | |||||
| Bed control | 37.00 (18.50-74.00) | 15.00 (4.00-59.00) | .076 | - | 25.50 (6.50-62.75) | − | ||||
| Bed rail | 54.00 (22.00-113.00) | 10.00 (3.50-46.00) | .000 | 54.00 (22.00-113.00) | 10.00 (3.50-46.00) | .049 | ||||
| Cart pull | 42.50 (18.00-65.00) | 16.00 (5.00-29.00) | .000 | 69.00 (9.75-1422.75) | 20.00 (8.50-48.50) | .310 | ||||
| Light switch | 156.00 (57.75-366.75) | 18.00 (7.00-44.00) | .000 | 223.00 (138.50-539.25) | 40.00 (11.00-144.00) | .000 | ||||
| Machine control | 152.00 (79.00-341.00) | 15.00 (7.00-54.00) | .000 | 100.50 (64.25-344.00) | 45.00 (8.00-150.00) | .004 | ||||
| Tray table | 78.00 (40.00-424.00) | 10.00 (5.00-27.00) | .001 | 115.00 (28.00-428.00) | 21.00 (5.50-79.00) | .036 | ||||
| Call button | 48.00 (41.00-149.00) | 4.00 (1.50-30.00) | .013 | 19.00 (19.00-19.00) | 47.00 (6.00-95.00) | .625 | ||||
| Total | 79.00 (32.50-234.50) | 14.00 (5.00-44.00) | .000 | 158.00 (48.00-376.00) | 26.00 (8.00-71.00) | .000 | ||||
Mann-Whitney U test.
† n = 1.
Discussion
Several literatures compared different methods to evaluate cleaning effectiveness. Overall, the highest clean rates were by visual inspection.
10
, 11
, 12
However, in Snyder et al's study, the highest clean rate was by microbiological method and the lowest clean rate was by fluorscent marker method.14
Hung et al. also found that the clean rate by fluorescent marker method was significantly lower than by microbiological method and ATP bioluminescence because residual gel on a surface could not be interpreted as the level of bioburden.15
In this study, “compliant,” “clean” and “pass” rates were 55.4%, 87.5, and 26.6% by performance observation, visual inspection and ATP interpretation with cutoff value 10 RLU, respectively. The highest rate was by visual inspection while the lowest rate was by ATP interpretation. There was no correlation between the results of visual inspection and ATP interpretation. We also found that clean rates by visual inspection tended to be overestimated compared to ATP interpretation and unassociated with each other.
10
, 11
, 12
That may result in regarding dirty surfaces as clean and spreading pathogens. The correlations between the results by visual inspection and performance observation and between performance observation and ATP interpretation were weak positive, indicating that the results of these 3 methods were not consistent and could not be inferred from each other. It may result from different contamination levels and wipe strength. Snyder et al also found that visual inspection, fluorescent marker, and ATP demonstrated poor correlation with microbiologic comparator and with each other.14
We found that the ATP readings were significantly lower in “compliant” and “clean” groups than in “ not compliant” and “ not clean,” but the correlations between any 2 methods were poor. The key point was the cutoff value of ATP bioluminescence to define “clean.” There were authors who followed manufacturer instructions to set the cutoff values, for example, <5 RLU was considered clean for 3M Clean-Trace System, <10 RLU was considered clean for Hygiena ATP Monitoring Systems in this study.
9
,Hygiena. UltraSnap surface ATP Test. Available at: file:///C:/Users/Vgh00/Downloads/INS0039%20-%20UltraSnap_RevC_All%20Languages.pdf. Accessed December 20, 2020.
12
There were authors who followed prior studies, for example, <250 RLU or <500 RLU were considered clean for 3 M Clean-Trace NG Luminometer and 3M Clean-Trace System.10
,14
,15
Several studies used microbiologic comparator, aerobic colony counts (ACC), to be the standard method to evaluate the effects of different methods in detecting cleanliness and showed no correlation, poor or moderate correlation between the ACC and ATP.
12
,13
,19
Many factors affect the ATP system, including bacteria species, colony counts, growth phase of bacteria, residual bleach solutions and material of environmental surfaces. The ATP system is relatively poor detection of gram-negative bacteria and in low colony counts less than 103
colony-forming unit.- Knelson L.P.
- Williams D.A.
- Gergen M.F.
- Rutala W.A.
- Weber D.J.
- Sexton D.J.
A comparison of environmental contamination by patients infected or colonized with methicillin-resistant Staphylococcus aureus or vancomycin-resistant Enterococci:a multicenter study.
Infect Control Hosp Epidemiol. 2014; 35: 872-875
20
, 21
In Fattorini et al's reserch, fluorescent marker was compared with ACC and showed no correlations.22
Besides, ATP can not only detect microbiological contaminants but also organic matter. That may explain why Sanna et al found that there was no correlation between ATP and total viable counts, but the 2 methods were consistent to identify the most contaminated areas.19
Results from the study, the highest mean ATP reading and the second lowest “compliant” rate were from the machine control panels. We found that most housekeepers were afraid to press any buttons accidentally and change the settings so that they did not wipe machine controls properly. The lowest mean ATP reading was from call buttons with the lowest “compliant” rate. That might be most patients were unconscious in the intensive care unit so housekeepers thought that the call buttons were not used.
Many studies tried to figure out which method was effective, rapid, and simple to assessment cleanliness. It would be better to give feedback to housekeepers on the spot. The results of performance observation have been rarely compared with other methods. However, the other methods, including visual inspection, ATP bioluminescence, aerobic colony counts and fluorescent marker, were often compared.
12
,13
,15
,22
Aerobic colony counts could quantify organism but it would be the most expensive, time-consuming method and needs to be executed by medical technician. ATP bioluminescence needs devices and training how to implement. Fluorescent marker is an indirect method to find out whether the surfaces are cleaned or not. Visual inspection would be the cheapest and easiest method. Studies indicated that the sensitivity of ATP was higher than visual inspection.12
,14
The clean rates of visual inspection were significantly higher than ATP.10
, 11
, 12
When the environment is visually clean, it would give people the first good impression. Griffith and Fattorini et al recommended that an integrated monitoring program or multistep process for assessing hospital cleanliness were needed.8
,22
That was using visual inspection or fluorescent markers first after appropriate cleaning. If surfaces are clean, using ATP bioluminescence in surfaces classified as high risk or critical surface.8
If ATP bioluminescence shows failure, surfaces need to be re-cleaned or detected by microbiological Methods.22
There are several limitations in the study. First, there is no objective standard for visual inspection, especially which old and faded surfaces. It is hard to maintain consistency visually even though a single nurse was assigned to assess cleanliness. Second, we did not use aerobic colony counts to be the comparator because the ATP value may be affected by the first swab. Therefore, there was no golden standard to be compared. Third, the optimal benchmark needs to be tested. Fourth, the residual bleach solutions and material of environmental surfaces may interfere with ATP results.
20
, 21
Conclusion
In conclusion, we have found that there was no correlation between visual inspection and ATP. The correlations were weak positive between visual inspection and performance observation, and between performance observation and ATP. Although the ATP readings were lower in “compliant” and “clean” groups than in “not compliant” and “not clean,” the best cutoff value needs to be established in this hospital. Considering the effectiveness, we recommended that a combined program would be preferred to include performance observation first, then testing by ATP in surfaces classified as high risk. In surfaces classified as low risk, using Visual inspection would be a rapid, and timesaving assessment tool.
References
- The role of colonization pressure in the spread of vancomycin-resistant Enterococci.Arch Intern Med. 1998; 158: 1127-1132
- Efficacy of a hospital-wide environmental cleaning protocol on hospital-acquired methicillin-resistant Staphylococcus aureus rates.J Infect Prev. 2016; 17: 171-176
- A comparison of environmental contamination by patients infected or colonized with methicillin-resistant Staphylococcus aureus or vancomycin-resistant Enterococci:a multicenter study.Infect Control Hosp Epidemiol. 2014; 35: 872-875
- Impact of environmental cleaning on the colonization and infection rates of multidrug-resistant Acinetobacter baumannii in patients within the intensive care unit in a tertiary hospital.Antimicrob Resist Infect Control. 2021; 10: 4
- An environmental cleaning bundle and health-care-associated infections in hospitals (REACH): a multicentre, randomised trial.Lancet Infect Dis. 2019; 19: 410-418
- Environmental cleaning and decontamination to prevent clostridioides difficile infection in health care settings:a systematic review.J Patient Safe. 2020; 16: S12-S15
Guh A., Carling P., Options for evaluating environmental cleaning. Available at: https://www.cdc.gov/hai/pdfs/toolkits/Environ-Cleaning-Eval-Toolkit12-2-2010.pdf. Accessed June 9, 2021.
- Methods to evaluate environmental cleanliness in healthcare facilities.Healthc Infect. 2013; 18: 23-30
Hygiena. UltraSnap surface ATP Test. Available at: file:///C:/Users/Vgh00/Downloads/INS0039%20-%20UltraSnap_RevC_All%20Languages.pdf. Accessed December 20, 2020.
- Finding a benchmark for monitoring hospital cleanliness.J Hosp Infect. 2011; 77: 25-30
- An evaluation of hospital cleaning regimes and standards.J Hosp Infect. 2000; 45: 19-28
- Comparing visual inspection, aerobic colony counts, and adenosine triphosphate bioluminescence assay for evaluating surface cleanliness at a medical center.Am J Infect Control. 2015; 43: 882-886
- Effectiveness of ATP bioluminescence to assess hospital cleaning: a review.J Prev Med Hyg. 2017; 58: E177-E183
- Effectiveness of visual inspection compared with non-microbiologic methods to determine the thoroughness of post-discharge cleaning.Antimicrob Resist Infect Control. 2013; 2: 26
- Application of a fluorescent marker with quantitative bioburden methods to assess cleanliness.Infect Control Hosp Epidemiol. 2018; 39: 1296-1300
Centers for Disease Control and Prevention. CDC environmental checklist for monitoring terminal cleaning. Available at: https://www.cdc.gov/hai/pdfs/toolkits/Environmental-Cleaning-Checklist-10-6-2010.pdf. Accessed December 20, 2020.
- Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay.Infect Control Hosp Epidemiol. 2009; 30: 678-684
SAGE Research Methods Datasets. Learn to use the phi coefficient measure and test in R with data from the welsh health survey. Available at: https://methods.sagepub.com/base/download/DatasetStudentGuide/phi-coefficient-whs-2009-r. Accessed December 20, 2020.
- ATP bioluminescence assay for evaluating cleaning practices in operating theatres: applicability and limitations.BMC Infect Dis. 2018; 18: 583-589
- Efficacy and limitations of an ATP-based monitoring system.J Am Assoc Lab Anim Sci. 2010; 49: 190-195
- ATP bioluminescence values are significantly different depending upon material surface properties of the sampling location in hospitals.BMC Res Notes. 2015; 8: 807-815
- Use of a fluorescent marker for assessing hospital bathroom cleanliness.Am J Infect Control. 2016; 44: 1066-1068
Article Info
Publication History
Published online: July 24, 2021
Footnotes
Conflict of interest: None.
Identification
Copyright
© 2021 The Author(s). Published by Elsevier Inc. on behalf of Association for Professionals in Infection Control and Epidemiology, Inc.
User License
Creative Commons Attribution (CC BY 4.0) | How you can reuse 
Elsevier's open access license policy
Creative Commons Attribution (CC BY 4.0)
Permitted
- Read, print & download
- Redistribute or republish the final article
- Text & data mine
- Translate the article
- Reuse portions or extracts from the article in other works
- Sell or re-use for commercial purposes
Elsevier's open access license policy
