American Journal of Infection Control 45 (2017) e69-e73

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American Journal of Infection Control American Journal of

Infection Control

j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g

Major Article

Effectiveness of cleaning-disinfection wipes and sprays against

multidrug-resistant outbreak strains
Nikki Kenters BSc a,*, Elisabeth G.W. Huijskens PhD, MD a,b, Sophie C.J. de Wit BSc a,
Joost van Rosmalen PhD c, Andreas Voss PhD, MD d,e
a
Department of Infection Prevention and Control, Albert Schweitzer Hospital, Dordrecht, The Netherlands
b
Department of Medical Microbiology, Albert Schweitzer Hospital, Dordrecht, The Netherlands
c Department of Biostatistics, Erasmus MC, Rotterdam, The Netherlands
d
Department of Medical Microbiology, Radboud University Medical Centre, Nijmegen, The Netherlands
e
Department of Medical Microbiology, Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands

Key Words: Background: Hospital rooms play an important role in the transmission of several health care–
Cleaning-disinfecting wipes associated pathogens. During the last few years, a number of innovative cleaning-disinfecting products
Cleaning-disinfecting sprays have been brought to market. In this study, commercially available products combining cleaning and dis-
Outbreak strains
infection were compared, using 2 different application methods. The aim was to determine which product
ATP
was most effective in simultaneous cleaning and disinfection of surfaces.
CFU
Methods: Seven cleaning-disinfecting wipes and sprays based on different active ingredients were tested
for their efficacy in removal of microbial burden and proteins. Efficacy was tested with known Dutch out-
break strains: vancomycin-resistant enterococci (VRE), Klebsiella pneumoniae OXA-48, or Acinetobacter
baumannii.
Results: For all bacteria, ready-to-use cleaning-disinfecting products reduced the microbial count with
a log10 reduction >5 with a 5-minute exposure time, with the exception of a spray based on hydrogen
peroxide. Omitting the aforementioned hydrogen peroxide spray, there were no significant differences
between use of a wipe or spray in bacterial load reduction. Using adenosine triphosphate (ATP) mea-
surements, a significant difference in log10 relative light units (RLU) reduction between various bacteria
(P ≤ .001) was observed.
Conclusions: In general, a >5 log10 reduction of colony forming units (CFU) for tested wipes and sprays
was obtained for all tested bacteria strains, with exception of hydrogen peroxide spray and VRE. Al-
though ATP may show a difference between pre- and postcleaning, RLU reduction does not correlate with
actual CFU reductions.
© 2017 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier
Inc. All rights reserved.

It is becoming apparent that cleaning and disinfection of patient
environments in hospitals is extremely important. Multidrug-
resistant microorganisms are emerging globally.1 Hospital rooms play
an import role in the transmission of several health care–associated
pathogens, including (methicillin-resistant) Staphylococcus aureus,
vancomycin-resistant enterococci (VRE), and norovirus.2 All these
microorganisms persist in the environment for an extended amount
of time.3 Research has shown that patients admitted to a hospital
room that was previously occupied by a patient that harbored a
* Address correspondence to Nikki Kenters, BSc, Albert Schweitzer Hospital, Albert
Schweitzerplaats 25, 3318 AT Dordrecht, The Netherlands.
E-mail address: n.kenters@gmail.com (N. Kenters).
Conflicts of interest: None to report.
health care–associated pathogen have a greater risk factor of getting
colonized or infected with the same pathogen.3
Improved terminal cleaning and disinfection of rooms leads to
decreased rates of pathogen transmission.4 Still, multiple studies have
demonstrated that <50% of hospital rooms are adequately cleaned
and disinfected when chemical germicides are used.4-6
Over the last few years, a number of innovative cleaning and dis-
infecting products have come on to the market. Ultraviolet
disinfection and hydrogen peroxide vapor devices are becoming
common in hospitals. These devices are an asset to terminal dis-
infection of patient rooms.7,8 Ready-to-use cleaning-disinfecting
wipes and sprays are becoming regular for cleaning and disinfec-
tion in hospitals. Ready-to-use products can be used for routine and
terminal cleaning and disinfection. The ease of use of the wipes and
sprays has the potential to save time and reduce barriers for health

0196-6553/© 2017 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ajic.2017.04.290
e70 N. Kenters et al. / American Journal of Infection Control 45 (2017) e69-e73

Table 1
Disinfecting-cleaning wipe and spray ingredients

Wipe-spray Composition* Product Manufacturer and manufacturer location

Wipe and spray A Glucoprotamin 26 g/100 g (1.5%) Incidin plus wipes Ecolab, Nieuwegein, The Netherlands
Wipe and spray B Hydrogen peroxide (Hi-speed H2O2): 15 mg/g (CAS 77-22-841) Aseptix Sterimax Aseptix, Loenen a/d Vecht, The Netherlands
Sporicide wipes
Wipe and spray C Ethanol 140 mg/g, propane-2-ol 100 mg/g; propane-1-ol 60 mg/g, Bacillol 30 tissues Hartmann, Nijmegen, The Netherlands
N-alkyl amino propyl glycine (CAS 1397 34-65-9) 5 mg/g
Spray D Didecyldimonium chloride, benzalkonium chloride, Formula 429 spray Formula 429, Amsterdam, The Netherlands
polyaminopropyl biguanide, dimethicone

*Active ingredient(s).

Table 2
care workers to apply these ready-to-use products. Because anti-
Mean log10 bacterial load reduction and mean log10 RLU reduction of cleaning-
microbial resistance is becoming a big threat for effective treating disinfection products with 95% CIs
of infections, cleaning and disinfection products are of great im-
Product Log10 CFU reduction Log10 RLU reduction
portance to reduce transmission between patients. Currently, there
is a lack of evidence that these products are truly effective in clean- Wipe A 5.77 (95% CI, 5.61-5.94) 1.98 (95% CI, 1.85-2.11)
Spray A 5.74 (95% CI, 5.58-5.90) 1.95 (95% CI, 1.82-2.08)
ing and disinfecting at the same time. The aim of this study was
Wipe B 5.58 (95% CI, 5.41-5.74) 2.27 (95% CI, 2.14-2.39)
to compare the effectiveness of commercially available products in Spray B 5.33 (95% CI, 5.16-5.49) 1.82 (95% CI, 1.69-1.94)
simultaneous cleaning and disinfection with 2 different applica- Wipe C 5.56 (95% CI, 5.40-5.73) 1.84 (95% CI, 1.71-1.97)
tion methods. Spray C 5.69 (95% CI, 5.53-5.85) 1.78 (95% CI, 1.65-1.91)
Spray D 5.72 (95% CI, 5.56-5.89) 1.60 (95% CI, 1.46-1.76)

MATERIALS AND METHODS CFU, colony forming units; CI, confidence interval; RLU, relative light unit.

Cleaning-disinfecting wipes and sprays

Seven cleaning-disinfecting wipes were obtained from differ-
ent manufacturers. The wipes and sprays are currently used in health
care facilities around Europe, except spray D is not yet, to our knowl-
edge, available. Specifications of wipes and sprays are summarized
in Table 1.
Bacteria isolates
Vancomycin-resistant Enterococcus faecium (isolate from 2013
outbreak at Canisius-Wilhelminia Hospital, The Netherlands), Kleb-
siella pneumoniae OXA-48 (isolate from 2011 outbreak at Maasstad
Hospital, The Netherlands), and Acinetobacter baumannii (ATCC,
Rockville, MD) were used as test organisms. Strains were grown over-
night at 37°C on blood agar.
Efficacy of cleaning-disinfectant products in removal of
microorganisms
Bacterial isolates were suspended in physiologic saline and ad-
justed to a McFarland standard of 0.5. Test organisms were then
added to 2 different test soils. All tests were performed in tripli-
cate, including a positive control per test organism. The colony
forming units (CFU) found in the positive control were used for
analysis.
The first test soil contained 3% bovine serum albumin with 0.3%
sheep erythrocytes, and the second test soil contained 12% bovine
serum albumin with 10% sheep erythrocytes.9 The test solution used
consisted of 1 mL of bacterial suspension, 0.2 mL of soil solution,
and 0.8 mL diluent. Standardized ceramic tiles (3709/PA00; Villeroy
& Boch, Mettlach, Saarland, Germany) measuring 5 × 5 cm were used
as the test surface. Tiles were sterilized before use. Tiles were con-
taminated with 0.1 mL of test suspension. Test suspension was evenly
spread over the whole area of the tile and was left to dry for 1 hour
at room temperature under laminar airflow.
To measure adenosine triphosphate (ATP), the tiles were swabbed
with a consistent pattern (up and down, left to right while the swab
was rotated). The swabs were then reinserted into their container
and allowed to react with the reagents in the cuvette for 10 seconds.
The swabs were placed into the Clean-Trace NG Luminometer (3M;
Neuss, North Rhine-Westphalia, Germany), and relative light units
(RLU) were recorded.
To measure CFUs, the contaminated tile was wiped with a cloth
or sprayed and then wiped with a paper towel with the products
described in Table 2. A single technician performed all tests. A stan-
dardized sweeping technique was used, starting in the left upper
corner performing a meander-like pattern, with 4 turns, ending in
the right lower corner.
The tile was then placed into the neutralizer. The neutralizer con-
sisted of lecithin 3 g/L, L-histidine 1 g/L, and saponin 30 g/L in diluent
(tryptone, pancreatic digest of casein 1.0 g/L, and sodium chloride
8.5 g/L). After 2 minutes of rest in the neutralizer (10 mL), and 3
minutes of horizontal shaking (150 rpm) with glass beads (15 g,
5 mm), an aliquot of the suspension was plated on tryptic soy agar.
After the incubation time of 24 hours at 37°C on tryptic soy agar,
CFU were counted.
To measure ATP after the treatment of cleaning-disinfection, prod-
ucts on the tile were swabbed again as previously described and
then recorded.
Statistical analyses
Analysis of variance was used with the log10 reduction of CFU
and RLU as the dependent variable and bacteria, wipes A-C and
sprays A-D, and level of soil (3% and 12%) as the independent vari-
ables. Two-way interaction effects of bacteria, wipe-spray, and level
of pollution were included in the model when statistically signif-
icant. Tukey method for multiple comparisons of means was used
to evaluate the differences between the different products and bac-
teria. The results of the analysis of variance models are presented
using estimated marginal means, which are the predicted values
of the dependent variable adjusted for the effects of the indepen-
dent variables. Association between CFU and RLU was assessed using
Spearman rank correlation. All statistical analyses were carried out
in R version 3.1.1 (R Core Team, Vienna, Austria), and a 2-sided sig-
nificance level of .05 was used.
 N. Kenters et al. / American Journal of Infection Control 45 (2017) e69-e73
RESULTS
In this study, different cleaning-disinfection products were used
to determine their effect on CFU reduction of VRE, A baumannii, and
K pneumoniae OXA-48 outbreak isolates and to evaluate their effect
on RLU reduction.
CFU reduction
The estimated marginal mean log10 CFU reduction for all prod-
ucts, with both the bacteria and 12% soil level, is shown in Figure 1
(data for 3% soil level is not shown). The CFU reduction for K
pneumoniae OXA-48 was larger (log10, 5.77; 95% confidence inter-
val [CI], 5.66-5.87) than for A baumannii (log10, 5.64; 95% CI, 5.54-
5.75) and VRE (log10, 5.46; 95% CI, 5.36-5.57). The different products
reached a 5 log10 CFU reduction against all tested microorganisms,
with the exception of spray B (CFU log10 reduction, 4.43) with VRE.
The marginal estimated mean log10 reduction of the tested prod-
ucts is shown in Table 2. Wipe A had the highest log10 CFU reduction
of 5.77 (95% CI, 5.61-5.94) and spray B the lowest log10 CFU reduc-
tion of 5.33 (95% CI, 5.16-5.49). In general, no significant difference
was found between the efficacy of the wipes and sprays with the
same active ingredient (product A, P < .99; product B, P = .32; product
C, P = .93), with the exception of the in vivo efficacy of product B
against VRE, for which the spray had a significantly lower efficacy
(P < .001).
ATP reduction
Different concentrations (3% and 12%) of test soil had no signif-
icant impact on RLU reduction (P = .08).
Using ATP measurements, a significant difference in log10 RLU
reduction between the various bacteria (P < .001) was observed. On
average, the RLU reduction of K pneumoniae OXA-48 (log10, 1.70; 95%
CI, 1.62-1.79) was lower than the RLU reduction of VRE (log10, 2.06;
Fig 1. Colony forming unit reduction with high environmental contamination. Mean log10 bacterial removal from tiles examining efficacy of disinfecting cleaning wipes
and spray with a 12% test soil against vancomycin-resistant enterococci, Klebsiella pneumoniae OXA-48, and Acinetobacter baumannii. Data are the estimated mean of 3 trip-
licates, and bars represent 95% prediction intervals.
e71
95% CI, 1.97-2.14) and A baumannii (log10, 1.90; 95% CI, 1.81-1.98).
The estimated marginal mean of RLU log10 reduction per bacteria
is shown in Figure 2 for the 12% soil level (data for 3% soil level is
not shown). Differences in efficacy in RLU log10 reduction are found
between the different types of products (P < .001) (Table 2). Wipe
B was found to be most effective in removing soil, with a RLU log10
reduction of 2.27 (95% CI, 2.14-2.39), whereas spray D with a re-
duction of 1.60 (95% CI, 1.47-1.73) was least effective. In general, RLU
reduction showed no significant difference between the identical
wipes and sprays (product A, P > .99; product B, P > .99). Only for
product B was a significant difference found (P < .001), where spray
B had a lower RLU reduction.
Correlation between CFU and RLU
Overall, no significant correlation between CFU and RLU was
found. The Spearman rank correlation coefficient was 0.024 for the
3% test soil (P = .85) and 0.04 for the 12% test soil (P = .73).
DISCUSSION
Different factors affect the efficacy of ready-to-use cleaning-
disinfecting sprays or wipes. In this study, cleaning practices were
mimicked in vitro. Secretion, excretion, and blood are often found
within the patient environment of health care facilities. These fluids
often contain microorganisms that can be harmful to health care
workers or patients. We executed a comparable experiment with
2 different test soils, low and high soil content, to mimic all pos-
sible clinical situations. The product instructions were followed as
described in the approved manual provided by the Board for the
Authorisation of Plant Protection Products and Biocides, The Neth-
erlands. The instructions provided for the wipes were to moisturize
the surface properly with the wipe to keep the surface moistened
for 5 minutes. The spray had to be used 30 cm from the surface and
then wiped with a paper towel or a cloth.
e72 N. Kenters et al. / American Journal of Infection Control 45 (2017) e69-e73
Fig 2. Adenosine triphosphate reduction (ATP) with high environmental contamination. Mean log10 ATP reduction from tiles examining efficacy of disinfecting-cleaning
wipes and spray with a 12% test soil against Acinetobacter baumannii, vancomycin-resistant enterococci, and Klebsiella pneumoniae OXA-48. Data are the estimated mean of
3 triplicates, and bars represent 95% prediction intervals.
For all bacteria, the tested ready-to-use cleaning-disinfection
products reduced the microbial count by >5 log10 with 5-minute ex-
posure time, with the exception of a spray based on hydrogen
peroxide. This hydrogen peroxide spray had an average 4.43 log10
CFU reduction on VRE. The test products are composed differently
and therefore are also charged differently, and the organic surfac-
tants may alter the physical properties of hydrogen peroxide in terms
of spreadability.
Overall, our results show low variability of the different wipes
and sprays in reducing bacterial counts. The Board for the Authori-
sation of Plant Protection Products and Biocides demands an efficacy
of a 5 log10 reduction in microbial count to get approval for the use
of a cleaning-disinfecting product.
According to testing standards, we used paper towels with the
sprays. Because of the mechanical properties of the ready-to-use
wipes in comparison with paper towels, some differences could have
been expected. Still, in a study by Diab-Elschahawi et al, no signif-
icant difference was found in the decontamination efficacy of
microfibers, cotton cloths, and paper towels.9
Wipes-based products are available in ready-to-use packaging
or as a solution that needs to be prepared in a reusable container
to impregnate the wipes. Ready-to-use wipes should be favored over
wipes in reusable tissue containers that need to be prepared. A study
by Kampf et al found that neglecting adequate processing of the con-
tainers contributed to frequent and heavy contamination.10 In
addition, there is a chance of preparing incorrect disinfection so-
lutions that are unnecessarily toxic or less effective. The sprays are
all ready-to-use, but have different factors that may change the ef-
ficacy (eg, application method [directly on the wipe or on the
surface]) and amount sprayed on a square centimeter. The usage
of sprays could lead to increased improper usage of the product.
No literature of standardized tests for cleaning-disinfection spray
is available to date. In addition, there is still a lack of research about
the safety implications for staff working with the spray.
Ready-to-use cleaning-disinfection products have the poten-
tial to increase cleaning compliance. Especially when compared
with the traditional bucket method, which involves preparing sus-
pensions and carrying around a bucket with disinfecting solution.
The ease of use of ready-to-use cleaning-disinfection products
removes this barrier. In a brief study by Wiemken et al, a signifi-
cant increase in cleaning compliance was shown with ready-to-
use cleaning-disinfection wipes.11 Regarding antimicrobial resistance,
basic cleaning and disinfection is increasingly important in clini-
cal areas. Standardized testing will provide users and infection
control and prevention teams with more confidence that the prod-
ucts work in accordance with the claims on the labels. Easier
methods for better compliance of cleaning and disinfection will
contribute to infection control and prevention in clinical settings.
A study by Alfa et al showed a reduction of health care–acquired
infections when compliance of 80% was reached with cleaning-
disinfection wipes.12
The results in this study show that the 2 outcome measures, bac-
tericidal effect as CFU reduction and protein residue as RLUs, did
not correlate. The CFU reduction was highest for K pneumoniae for
all tested products, whereas the RLU reduction was lowest for K
pneumoniae. K pneumoniae produces a layer of polysaccharide, which
forms a biofilm on surfaces.13-15 The layer of polysaccharide helps
the bacteria to adhere to surfaces, which presumably makes it harder
to clean a surface properly. E faecium had on average the lowest CFU
reduction, but the highest RLU reduction. E faecium is a gram-
positive bacterium, which possibly has a higher tolerating desiccation
against disinfectants. Although the exact reasons are unknown, the
different bacterial properties obviously influence the results re-
garding CFU and RLU reduction.
In other studies, a correlation was shown between aerobic colony
count and ATP when surfaces were contaminated with
microorganisms.16-18 Within the clinical setting, microbial testing
of surfaces is expensive and time consuming and therefore only used
 N. Kenters et al. / American Journal of Infection Control 45 (2017) e69-e73
in limited settings.17,19 However, ATP testing is quick and easy to prac-
tice on hospital surfaces. Unfortunately, ATP meters from different
suppliers have different sensitivities and can also react with the de-
tergent, which makes it hard to set a threshold for this measurement.
Biocides often quench the ATP signal (indicating a low RLU), whereas
the presence of an organic load may increase the RLU value sig-
nificantly. Several quality standards have been used as RLU
thresholds, ranging from 100-500.16,17,20 A standardized quality stan-
dard needs to be developed. The fact that the 2 methods did not
correlate in our study does not implicate that they are not both
helpful for the purpose of auditing cleaning within the health care
setting.
The variety of different cleaning-disinfection products brought
to market makes testing the effectiveness a very elaborate process.
At the time the research was carried out, standardized methods for
surface disinfectants using cloths were not available. Now, 2 stan-
dards, the European test norm EN 16615 (4-field test) and the
international test norm ASTM E2967-15 (wiperator), are available.
Both methods demonstrate the compatibility of the cloth and the
active substance of the cloth. In addition, the 4-field test can give
statements on the area’s performance and distribution into the en-
vironment. However, Pseudomonas aeruginosa used as a test organism
in the standard has a loss of CFU caused by drying that can influ-
ence the test results.
The pressure of the wiperator is currently not yet comparable
with real-life situations. In October 2015, a study by Sattar et al
evaluated the new ASTM standard test protocol to demonstrate
efficacy of disinfectant wipes.21 Sattar et al states that the
developed standard is appropriate to assess the efficiency of
disinfection wipes. The wiperator ensures greater precision and
reproducibility.
A missed opportunity of the standards is not including a stan-
dardized testing method for sprays because they are increasingly
used in health care facilities.
The testing methods used in ASTME2967-15 and EN 16615
mainly differ in, manual versus machine wiping, horizontal
wiping versus circling wiping, and as well in contact pressure and
the duration of the application on surfaces. Both test methods
should be used in the future by manufacturers to assess the
disinfectant wipes to make more reliable claims. Clinical studies
are needed to assess if using ready-to-use wipes leads to a
reduction in the transmission of several health care–associated
pathogens.
In general, the log reduction of CFU for all tested wipes and
sprays was (with the mentioned exception) >5 log10 and therefore
appropriate for clinical use. Although ATP may show a difference
between pre- and postcleaning, RLU reduction does not correlate
with actual CFU reductions. A clinical study in a health care setting
would be an asset to prove efficiency of cleaning-disinfection wipes
and sprays.
e73
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