Use of ATP Readings to Predict a Successful Hygiene Intervention in the Workplace to Reduce the Spread of Viruses on Fomites

Abstract

The purpose of this study was to validate the use of adenosine triphosphate (ATP) for evaluating hygiene intervention effectiveness in reducing viral dissemination in an office environment. The bacterial virus MS-2 was used to evaluate two scenarios, one where the hand of an individual was contaminated and another where a fomite was contaminated. MS-2 was selected as a model because its shape and size are similar to many human pathogenic viruses. Two separate experiments were conducted, one in which the entrance door push plate was inoculated and the other in which the hand of one selected employee was inoculated. In both scenarios, 54 selected surfaces in the office were tested to assess the dissemination of the virus within the office. Associated surface contamination was also measured employing an ATP meter. More than half of the tested hands and surfaces in the office were contaminated with MS-2 within 4 h. Next, an intervention was conducted, and each scenario was repeated. Half of the participating employees were provided hand sanitizer, facial tissues, and disinfecting wipes, and were instructed in their use. A significant (p < 0.05) reduction was observed in the number of surfaces contaminated with virus. This reduction in viral spread was evident from the results of both viral culture and the surface ATP measurements, although there was no direct correlation between ATP measurements with respect to viral concentration. Although ATP does not measure viruses, these results demonstrate that ATP measurements could be useful for evaluating the effectiveness of hygiene interventions aimed at preventing viral spread in the workplace.

Full text

ORIGINAL PAPER
Use of ATP Readings to Predict a Successful Hygiene Intervention
in the Workplace to Reduce the Spread of Viruses on Fomites
Laura Y. Sifuentes
1
•Sonia L. M. Fankem
1
•Kelly Reynolds
1,2
•Akrum H. Tamimi
1
•
Charles P. Gerba
1
•David Koenig
3
Received: 20 July 2016 / Accepted: 11 August 2016
ÓSpringer Science+Business Media New York 2016
Abstract The purpose of this study was to validate the use
of adenosine triphosphate (ATP) for evaluating hygiene
intervention effectiveness in reducing viral dissemination
in an office environment. The bacterial virus MS-2 was
used to evaluate two scenarios, one where the hand of an
individual was contaminated and another where a fomite
was contaminated. MS-2 was selected as a model because
its shape and size are similar to many human pathogenic
viruses. Two separate experiments were conducted, one in
which the entrance door push plate was inoculated and the
other in which the hand of one selected employee was
inoculated. In both scenarios, 54 selected surfaces in the
office were tested to assess the dissemination of the virus
within the office. Associated surface contamination was
also measured employing an ATP meter. More than half of
the tested hands and surfaces in the office were contami-
nated with MS-2 within 4 h. Next, an intervention was
conducted, and each scenario was repeated. Half of the
participating employees were provided hand sanitizer,
facial tissues, and disinfecting wipes, and were instructed
in their use. A significant (p\0.05) reduction was
observed in the number of surfaces contaminated with
virus. This reduction in viral spread was evident from the
results of both viral culture and the surface ATP mea-
surements, although there was no direct correlation
between ATP measurements with respect to viral concen-
tration. Although ATP does not measure viruses, these
results demonstrate that ATP measurements could be use-
ful for evaluating the effectiveness of hygiene interventions
aimed at preventing viral spread in the workplace.
Keywords Hygiene Adenosine triphosphate (ATP) 
Viral dispersion Workplace Intervention MS-2 virus
Introduction
Enteric and respiratory illnesses are readily spread among
persons working together in an office environment, and can
result in significant economic and productivity losses
(Bramley et al. 2002; Birbaum et al. 2003; Callan et al.
2005). Although implementation of hygiene interventions
may reduce the spread of viral illnesses in the workplace,
traditional methods for evaluating their effectiveness are
costly and time-consuming. Rapid methods for screening
of relative biological loads on surfaces could be helpful in
evaluating the efficacy of mitigation efforts. In this study,
the measurement of ATP was used to determine its value as
a rapid screening method for evaluation of workplace
hygiene interventions in reducing the potential for viral
spread.
Common illnesses of viral etiology, such as colds and
diarrhea, have a significant impact on health care costs and
absenteeism among office employees (Bramley et al.
2002). The increasingly globalized economy creates
greater opportunity than ever before for viral transmission,
as evidenced by the recent and emerging viral pandemics
such as those caused by H1N1 (Swine Flu), H7N9 (Avian
&Charles P. Gerba
gerba@ag.arizona.edu
1
Department of Soil, Water and Environmental Science,
College of Agriculture and Life Sciences, The WEST Center,
Kimberly-Clark Corporation, University of Arizona, 2959 W.
Calle Agua Nueva, Tucson, AZ 85721, USA
2
Department of and Environmental Occupational Health,
College of Public Health, University of Arizona, Tucson,
AZ 85721, USA
3
Kimberly-Clark Corporation, 2100 Winchester Road,
Neenah, WI 54956, USA
123
Food Environ Virol
DOI 10.1007/s12560-016-9256-2

Flu), and norovirus (Cauchemez et al. 2009; Morens et al.
2013; Hall et al. 2013). Even if an employee is not absent
as a result of viral infection, the increased cost of signifi-
cantly reduced productivity can equal or exceed those of
absenteeism attributed to illness (Lamb et al. 2006).
In these relatively enclosed environments, commonly
touched surfaces, such as break room tables, photocopying
machines, door entrances, and restrooms, represent the
most likely routes for the spread of enteric and respiratory
viruses (Boone and Gerba 2007). Fomites, inanimate
objects or surfaces that serve as microbial transmission
vehicles, are contaminated by infected individuals through
either direct contact or by the settling of aerosols created
by sneezing or coughing. The viruses are then transferred
to the hands of the individuals touching these surfaces, and
are subsequently introduced to the site of infection (i.e.,
nose, mouth, or eyes). Nicas and Jones (2009) found that
adults contact these critical points of microbial entry to the
human body approximately 16 times each hour. Because
viruses can survive on fomites from a few hours to a month
(Boone and Gerba 2007), contaminated surfaces represent
an important means of infectious disease transmission.
Bacterial viruses (phages), which do not infect humans,
have been used to study the movement of viruses in indoor
environments such as day care centers, neonatal nurseries,
and home settings (Rheinbaben et al. 2000; Gerhardts et al.
2012; Lopez et al. 2013). The bacterial virus MS-2 was
used in this study to represent pathogenic virus spread in
the office environment. MS-2 infects the bacterium
Escherichia coli and is very similar in shape and size
(23 nm) to rhinovirus, norovirus (most common cause of
adult gastroenteritis), and many other enteric viruses. In
addition to studying viral transmission patterns, bacterio-
phage models are also useful in the validation of preventive
measures (Mamane-Gravetz and Linden 2004).
Availability and use of hygiene interventions have been
shown effective in the disruption of both direct contact and
surface-mediated microbial transmission in school and
hospital environments (Liu et al. 2009; Bright et al. 2010;
Bloomfield et al. 2016). Preventive measures such as hand
washing (Ryan et al. 2001;Curtis and Cairncross 2003) and
use of hand sanitizers (Sandora et al. 2005), as well as anti-
microbial wipes and cleaners (Kochar et al. 2009), have
been demonstrated to reduce gastrointestinal and respira-
tory infectious disease incidence. In addition, proper uses
of disposable surgical masks and facial tissues have been
used to reduce transmission of respiratory infections
through aerosolization. Although these measures have been
shown effective when properly implemented, there is not
currently a rapid, cost-effective means to routinely monitor
their sustained effectiveness.
Adenosine triphosphate (ATP), the universal energy
molecule found in all animal, plant, bacterial, yeast, and
mold cells, produces bioluminescence that has been sug-
gested as a potential alternative for rapid confirmation of
hygiene intervention effectiveness. ATP detection methods
have been validated for assessment of relative microbial
presence in aquatic environments (Hammes et al. 2010)
and intravenous fluids (Anderson et al. 1986), as well as on
inanimate surfaces in hospitals (Moore et al. 2010; Aikin
et al. 2011) and food preparation areas (Aycicek et al.
2006). ATP is thus used as a general indicator of cleanli-
ness of a surface. Simple, hand held, ATP meters are now
available that allow for testing of fomites with results
available in 15 s (Hygienia 2016). This creates an oppor-
tunity for rapid screening of fomites with minimum cost
and time.
This study describes the effectiveness of a workplace
hygiene intervention in preventing the spread of a bacterial
virus in an office environment as a model for removal of a
pathogenic virus. ATP measurements were then compared
to viral load after the implementation of the hygiene
intervention to determine if the general cleanliness of a
surface could be correlated with the removal of viral
pathogens. This could provide an alternative monitoring
tool for the simple and rapid confirmation of the effec-
tiveness of a hygiene intervention on reducing the spread of
viruses in the workplace.
Materials and Methods
Study Approach
MS-2 was used to evaluate two scenarios, one where the
hand of one selected employee was contaminated and
another where a fomite, the entrance door push plate, was
contaminated. Samples from 54 selected surfaces were
sampled in the office setting at the beginning of the day and
at 4 and 7 h after inoculation to assess the dissemination of
the virus within the office. The samples were subsequently
tested using traditional viral culture and ATP detection
methods to assess the spread of the virus through the office
environment from each of the two starting points. Each
experiment was repeated after the employees were
instructed on the use of provided hygiene interventions
including facial tissues, disinfecting wipes, and hand san-
itizer, as well as hand-washing techniques using basic (not
labeled as anti-microbial) hand soap.
Office Description
This study was conducted in an office setting with
approximately 80 full-time employees. The office is loca-
ted on the second floor of a three-story building, with three
stairway accesses and one elevator access to the floor. The
Food Environ Virol
123

main entry door to the floor is located near the elevator,
such that persons exiting the elevator enter through the
main door. The entire office shares a common kitchen area
(break room) equipped with a microwave oven, a sink area,
a coffee machine, and a refrigerator. Other features include
several individual offices with doors located along the
perimeter of the floor, a central area divided into cubicles,
and seven locations containing shared photocopy
machines. A floor plan of the office can be seen in Fig. 1.
MS-2 Virus
MS-2 (ATCC 15597-B1) was obtained from the American
Type Culture Collection (ATCC Manassas, VA). MS-2
virus was prepared as previously described with minor
modifications (Rusin et al. 2002). The agar overlay tech-
nique was used to isolate and enumerate phage MS-2.
Dilutions of sample suspension (1 mL) followed by log-
phase host culture (1 mL) were added to melted top agar
tubes. The inoculated top agar tubes were mixed and
poured over a TSA plate, and then the solidified agar
overlay was inverted and incubated at 37 °C for 24 h.
Phage plaques were counted, and the concentration of
phage isolated per 100 cm
2
was calculated for each fomite
sampled.
ATP Detection
ATP bioluminescence was measured in relative light units
(RLU) using a SystemSURE
TM
ATP meter (Hygiena,
Camarillio, CA) according to the manufacturer’s recom-
mended protocol. An adjacent 100 cm
2
to where the phage
sample was collected was swabbed with the swabs pro-
vided by the manufacturer for use with the device.
Surface Inoculation
An area of approximately 50 cm
2
on an office entrance
door push plate and the hand of one of employee were
inoculated with 6 910
9
/cm
2
plaque forming units (PFU)
of MS-2 bacterial virus. This was done before the arrival
of any of the employees to ensure they were unaware of
the inoculation. This level of phage was used to make it
easily traceable through the facility and not necessarily to
reflect an actual viral load from an infected person.
However, this level is not out of reality as persons
infected with adenovirus, rotavirus, and norovirus may
have 10
11
–10
12
virus particles per gram of feces (Maier
et al. 2009). Thus, 10
9
would represent only 0.01–0.001
grams of fecal material.
Sample Collection
Samples from 54 selected fomites and the hands of 42
participating employees were collected for viral assays
using sterile cotton transport swabs containing a buffer
to neutralize any residual disinfectant used on the sur-
face or hand (3 M Corporation, St. Paul, MN). Fomites
sampled included desk tops, table tops, refrigerator door
handles, microwave oven door handles, coffee pot han-
dles, and vending machine buttons. (Reynolds et al.
2016). Fomite samples for ATP detection were also
collected from adjacent surface areas using swabs rec-
ommended by the manufacturer for use with the Sys-
temSURE
TM
ATP meter (Hygiena, Camarillio, CA).
Each swab was aseptically removed from its transport
container, swabbed over an area of approximately
100 cm
2
for each surface, and carefully returned to its
transport container.
Fig. 1 Office floor plan
Food Environ Virol
123

The Healthy Workplace Project Intervention
Individual offices and communal areas were provided with
a series of intervention products intended to reduce the
spread of virus. The hygiene intervention was evaluated by
conducting the same inoculation and sampling protocol
before and after its implementation. The following prod-
ucts were provided for each individual office of these
individuals who agreed to participate in the intervention: a
bactericidal hand sanitizer (KIMTECH Moisturizing
Instant Hand Sanitizer, Kimberly-Clark Professional,
Roswell, GA), virucidal and bactericidal surface disin-
fecting wipes (SCOTT
Ò
Disinfectant Wipes, Kimberly-
Clark Professional, Roswell, GA), and facial tissue
(KLEENEX
Ò
Tissue, Kimberly-Clark Corporation, Nee-
nah, WI). Of the 80 persons in the office, 42 agreed to take
part in the intervention study.
Restrooms were stocked with basic hand soap (not anti-
bacterial) and paper towels. The communal areas were
provided with a bactericidal hand sanitizer with stands/
dispensers (KLEENEX
Ò
Moisturizing Instant Hand Sani-
tizer, Kimberly-Clark Global Sales, Roswell, GA). The
break room was provided with food safe bactericidal san-
itizing wipes (KIMTECH PREP* Surface Sanitizer Wipes,
Kimberly-Clark Professional, Roswell, GA), and the con-
ference rooms were equipped with a bactericidal hand
sanitizer (KIMTECH* Moisturizing Instant Hand Sanitizer,
Kimberly-Clark Professional, Roswell, GA), virucidal and
bactericidal surface disinfecting wipes (SCOTT
Ò
Disin-
fectant Wipes, Kimberly-Clark Professional, Roswell,
GA), and facial tissue (KLEENEX
Ò
Tissue, Kimberly-
Clark, Neenah, WI).
Employees were instructed on the implementation of the
Healthy Workplace Project. They were advised to sanitize
hands when entering and leaving the office, as well as
before and after shaking hands, after touching communal
surfaces, and after touching the nose or face. In addition,
they were provided with tissues to wipe or blow their
noses, and instructed to wash their hands for 15 s with soap
and dry with a clean paper towel after using the restroom
and before eating food. Employees were advised to use
disinfecting wipes to clean desk areas (keyboard, mouse,
and phone) at the beginning of each day and to wipe down
the conference room table before starting a meeting; and to
use sanitizing wipes to clean frequently touched items in
the break room such as refrigerator handles, microwave
handles and buttons, coffee pot handles, vending machine
buttons, and tables.
Statistical Analysis
Adenosine triphosphate (ATP) measurements taken before
and after the intervention were compared with results from
the viral culture analysis to identify any statistical corre-
lations. The statistical analysis was performed using
Microsoft
Ò
Excel
Ò
2010 (Microsoft Corporation, Red-
mond, WA). The data were plotted to determine whether it
followed a normal distribution model. The log-transformed
data (log
10
) were normally distributed, which allowed us to
perform the Analysis of Variance (ANOVA) with the
assumption of normal distribution. In order to answer
specific questions, multiple ANOVA tests were conducted
on the data to test different hypotheses. Completely ran-
domized designs were used to perform the ANOVA, with a
rejection region of 5 % using the Fdistribution.
Results
In order to evaluate the effectiveness of a hygiene inter-
vention for the reduction of MS-2 in an office setting, 54
samples were collected from commonly touched surfaces
for two baseline experiments and two interventions. Cor-
relations between the viral data and ATP measurements
were used to evaluate ATP as a rapid indicator of the
success of the intervention. No bacterial viruses were
detected on the fomites before the beginning of the study
(i.e., no background virus was recovered). MS-2 was
observed to spread throughout the office setting rapidly,
within 4 h, to a variety of fomites. Before implementation
of The Healthy Workplace Project, MS-2 virus had spread
to approximately 56 % of the fomites sampled within 4 h
after inoculation of one employee’s hand (Fig. 2), and
increased to 63 % at 7 h after inoculation.
Implementation of The Healthy Workplace Project
resulted in a reduction of MS-2 on fomites. The virus was
detected on 9 % of the fomites after 4 h and 30 % after 7 h
(Fig. 2). After 7 h, the number of contaminated fomites
and hands increased, but was still half as much that was
observed on the surfaces before the intervention (Fig. 3).
When the door push plate was contaminated, there were
Fig. 2 Percent positive of MS-2 occurrence on surfaces before and
after intervention
Food Environ Virol
123

70 % fewer fomites contaminated after 4 h during the
intervention portion of the study. Thus, there was a sig-
nificant overall reduction in virus occurrence on both hand
and fomite surfaces after implementation of The Healthy
Workplace Project.
A statistically significant difference was observed
between MS-2 concentrations with no intervention and
intervention experiments on fomites at the 4 h sampling
time (p\0.005). Using the ANOVA test with a 5 %
rejection region, the differences between pre-intervention
concentrations of MS-2 and those observed after a 7-h
workday remained marginally significant (p=0 054).
Combined data from both the 4 and 7 h time points
demonstrated that the impact of the intervention was highly
significant for reducing the exposure to MS-2 (Fig. 2). The
number of sites with an ATP reading of greater than 2 RLU
was 45 % before the intervention and 15 % after the
intervention. This difference was shown to be statistically
significant (p\0.005). Thus, ATP readings were useful in
determining the success of the hygiene intervention as they
demonstrated a significant reduction of virus on the sam-
pled fomites after the intervention.
Discussion and Conclusions
ATP bioluminescence is a general measurement of bio-
logical contamination. It does not directly monitor viruses,
but indicates a mixture of biological forms, such as human
cellular materials, bacteria, and plant and fungal cells.
Materials like epithelium from the upper respiratory tract
mucus membranes, saliva, and associated material from the
coughs and sneezes of persons with viral or bacterial
infections can also contribute to ATP measurements
(Shaughnessy et al. 2013).While there are limits to the use
of ATP measurements in assessing the impact of cleaning
practices (Green et al. 1999), recent studies have demon-
strated its potential usefulness for validating the effec-
tiveness of cleaning practices in schools (Shaughnessy
et al. 2013) and hospitals (Boyce et al. 2009a,b).
The rapid spread of virus throughout the office after a
high-touch surface (office door bar) or the hand of one
employee was inoculated illustrates how a contaminated
surface can result in viral transmission in the workplace.
Shared facilities (e.g., break room, copy machine), where
transfer of viruses from infected to uninfected persons is
most likely to occur, were readily contaminated. The viral
culture results show statistically significant reductions in
the spread of virus (MS-2) from either a contaminated hand
or fomite throughout an office environment after imple-
mentation of hygiene interventions. This was accomplished
with only 52 % of the occupants of the building partici-
pating in the intervention, demonstrating that a significant
reduction in virus spread can occur without everyone in the
office following the intervention protocol. In addition, this
improvement occurred after the intervention protocol was
in place for only 3 days before the virus was seeded onto
the hands/push plate. The seeding of the door handle or
hand of an employee made no significant difference in the
spread of the virus throughout the facility or the success of
the intervention (Reynolds et al. 2016). ATP measurements
correlated significantly with reduced viral recovery and
showed statistically significant differences in measure-
ments taken before and after an intervention. This suggests
that although ATP readings do not specifically predict the
occurrence or degree of reduction in microbial contami-
nation, the method can be useful for monitoring the success
of health interventions in the workplace in terms of the
reduction in the spread of a virus.
Despite the described limitations of ATP measurement
as a method for monitoring microbial contamination, the
resultsofthisstudyclearly demonstrate that workplace
hygiene interventions can result in a significant reduction
of viral contamination, and ATP can be used to monitor
performance rapidly. It also illustrates that a general
measure of cleanliness with a quantitative tool can be
related to the spread of viruses in indoor environments
and can be used as an aid to assess of potential inter-
ventions .
References
Aikin, Z. A., Wilson, M., & Pratten, J. (2011). Evaluation of ATP
bioluminescence assays for potential use in a hospital setting.
Infection Control and Hospital Epidemiology, 32, 507–509.
Anderson, R. L., Highsmith, A. K., & Holland, B. W. (1986).
Comparison of the standard pour plate procedure and the ATP
and limulus amebocyte lysate procedures for the detection of
microbial contamination in intravenous fluids. Journal of
Clinical Microbiology, 23, 465–468.
Aycicek, H., Oguz, U., & Karci, K. (2006). Comparison of results of
ATP bioluminescence and traditional hygiene swabbing methods
for the determination of surface cleanliness at a hospital kitchen.
Fig. 3 Virus concentrations per 100 cm
2
on surfaces (n=54) and
ATP relative light units (RLU) before and after intervention
Food Environ Virol
123

International Journal of Hygiene and Environmental Health,
209, 203–206.
Birbaum, H., Morley, M., Leong, S., & Colice, G. (2003). Lower
respiratory tract infections: impact on the workplace. Pharma-
coeconomics, 21, 749–759.
Bloomfield, S. F., Exner, M., Signorelli, C., Nath, K. J., & Scott E. A.
(2016). The chain of infection transmission in the home and
everyday life settings, and the role of hygiene in reducing the
risk of infection. http://www.ifh-homehygiene.org/Integra
tedCRD.nsf/111e68.
Boone, S. A., & Gerba, C. P. (2007). Significance of fomites in the
spread of respiratory and enteric viral disease. Applied and
Environmental Microbiology, 73, 1687–1696.
Boyce, J. M., Havell, H. L., Dumigan, D. G., Golebiewski, M.,
Balogun, O., & Rizvani, R. (2009a). Monitoring the effective-
ness of hospital cleaning practices by use of an adenosine
triphosphate bioluminescence assay. Infection Control and
Hospital Epidemiology, 30, 678–684.
Boyce, J. M., Havell, H. L., Dumigan, D. G., Golebiewski, M.,
Balogun, O., & Rizvani, R. (2009b). Monitoring the effective-
ness of hospital cleaning practices by use of an adenosine
triphosphate bioluminescence assay. Infection Control and
Hospital Epidemiology, 30, 678–684.
Bramley, T. J., Lermer, D., & Sarnes, M. (2002). Productivity loses
related to the common cold. Journal of Occupational Environ-
mental Medicine, 44, 822–829.
Bright, K. R., Boone, S. A., & Gerba, C. P. (2010). Occurrence of
bacteria and viruses on elementary classroom surfaces and the
potential role of classroom hygiene in the spread of infectious
diseases. Journal of School Nursing, 26, 33–41.
Callan, E., Majowicz, S. F., Hall, G., Banerjee, A., Bowman, C. L.,
et al. (2005). Prevalence of diarrhea in the community in
Australia, Canada, Ireland, and the United States. International
Journal of Epidemiology, 34, 54–460.
Cauchemez, S., Donnelly, C. A., Reed, C., Ghani, A. C., Fraser, C.,
Kent, C. K., et al. (2009). Household transmission of 2009
pandemic influenza A (H1N1) in the United States. New England
Journal of Medicine, 361, 2619–2627.
Curtis, V., & Cairncross, S. (2003). Effect of washing hands with soap
on diarrhea risk in the community: a systematic review. The
Lancet Infectious Diseases, 3, 275–281.
Gerhardts, A., Hammer, T. R., Balluff, C., Mucha, H., & Hoefer, D.
(2012). A model of the transmission of micro-organisms in a
public setting and its correlation to pathogen infection risks.
Journal of Applied Microbiology, 112, 614–621.
Green, T. A., Russell, S. M., & Fletcher, D. L. (1999). Effect of chemical
cleaning agents and commercial sanitizers on ATP bioluminescence
measurements. Journal of Food Protection, 62, 86–90.
Hall, A. J., Lopman, B. A., Payne, D. C., Patel, M. M., Gastan
˜aduy, P.
A., Vinje
´, P., et al. (2013). Norovirus disease in the United
States. Emerging Infectious Disease, 19, 1198–1205.
Hammes, F., Goldschmidt, F., Vital, F., Wang, Y., & Egli, T. (2010).
Measurement and interpretation of microbial adenosine tri-
phosphate (ATP) in aquatic environments. Water Research, 44,
3915–3923.
Hygienia. (2016). www.hygienia.com. Accessed 4 August 2016.
Kochar, S., Heard, T., Sharma, R., Hui, A., Tolentino, E., Allen, G.,
et al. (2009). Success of an infection control program to reduce
the spread of carbapenem-resistant Klebsiella pneumoniae.
Infection Control and Hospital Epidemiology, 30, 447–452.
Lamb, C. E., Ratner, P. H., Johnson, C. E., Ambegaonkar, A. J., Joshi,
A. V., Day, D., et al. (2006). Economic impact of workplace
productivity losses due to allergic rhinitis compared with select
medical conditions in the United States from an employer
perspective. Current Medical Research Opinion, 22, 1203–1210.
Liu, P., Yuen, Y., Hsiao, H. M., Jaykus, L. A., & Moe, C. (2009).
Effectiveness of liquid soap and hand sanitizer against Norwalk
virus on contaminated hands. Applied and Environmental
Microbiology, 76, 394–399.
Lopez, G. U., Gerba, C. P., Tamimi, A. H., Kitajima, M., Maxwell, S.
L., & Rose, J. B. (2013). Transfer efficiency of bacteria and
viruses from porous and nonporous fomites to fingers under
different relative humidity. Applied and Environmental Micro-
biology, 79, 728–5734.
Maier, R. M., Pepper, I. L., & Gerba, C. P. (2009). Environmental
microbiology. San Diego: Academic Press.
Mamane-Gravetz, H., & Linden, K. G. (2004). UV disinfection of
indigenous aerobic spores: implications for UV reactor valida-
tion in unfiltered waters. Water Research, 38, 2898–2906.
Moore, G., Smyth, D., Singleton, J., & Wilson, P. (2010). The use of
adenosine triphosphate bioluminescence to assess the efficacy of
a modified cleaning program implemented within an intensive
care setting. American Journal of Infection Control, 38,
617–622.
Morens, D. M., Taubenberger, J. K., & Fauci, A. S. (2013). Pandemic
influenza viruses—hoping for the road not taken. New England
Journal of Medicine, 368, 2345–2348.
Nicas, M., & Jones, R. M. (2009). Relative contributions of four
exposure pathways to influenza infection risk. Risk Analysis, 29,
1292–1303.
Reynolds, K. A., Beamer, P. I., Plotkin, K. R., Sifuentes, L. Y.,
Koenig, D. W., & Gerba, C. P. (2016). The healthy workplace
project: reduced viral exposure in an office setting. Archives of
Environmental & Occupational Health, 71, 157–162.
Rheinbaben, F., Schunemann, S., Gross, T., & Wolff, M. H. (2000).
Transmission of viruses via contact in a household setting:
experiments using bacteriophage straight phiX174 as a model
virus. Journal of Hospital Infection, 46, 61–66.
Rusin, P., Maxwell, S., & Gerba, C. (2002). Comparative surface-to-
hand and fingertip-to-mouth transfer efficiency of gram-positive
bacteria, gram-negative bacteria, and phage. Journal of Applied
Microbiology, 93, 585–592.
Ryan, M. A. K., Christian, R. S., & Wohlrabe, J. (2001). Handwash-
ing and respiratory illness among young adults in military
training. American Journal of Preventive Medicine, 21, 79–83.
Sandora, T. J., Taveras, E. M., Shih, M. C., Resnick, E. A., Lee, G.
M., et al. (2005). Alcohol-based hand sanitizer and hand-hygiene
education to reduce illness transmission in the home. Pediatrics,
116, 587–594.
Shaughnessy, R. J., Cole, E. C., Moschandreas, D., & Haverinen-
Shaughnessy, U. (2013). ATP as a marker for surface contam-
ination of biological origin in schools and as a potential approach
to the measurement of cleaning effectiveness. Journal of
Environmental Health, 10, 336–346.
Food Environ Virol
123