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Indoor Air 2015; 25: 694–707 © 2015 The Authors.

© 2015 The Authors. Indoor Air Published by John Wiley & Sons Ltd.
wileyonlinelibrary.com/journal/ina
Printed in Singapore. All rights reserved INDOOR AIR
doi:10.1111/ina.12186

Modeling environmental contamination in hospital single- and


four-bed rooms

Abstract Aerial dispersion of pathogens is recognized as a potential M-F. King, C. J. Noakes,


transmission route for hospital acquired infections; however, little is known P. A. Sleigh
about the link between healthcare worker (HCW) contacts’ with contaminated
surfaces, the transmission of infections and hospital room design. We combine School of Civil Engineering, Pathogen Control
computational fluid dynamics (CFD) simulations of bioaerosol deposition with Engineering Institute, University of Leeds, Leeds, UK
a validated probabilistic HCW–surface contact model to estimate the relative
Key words: HCAI; Indirect transmission; Hand contami-
quantity of pathogens accrued on hands during six types of care procedures in nation; CFD; Markov chain; Bioaerosol.
two room types. Results demonstrate that care type is most influential
(P < 0.001), followed by the number of surface contacts (P < 0.001) and the
distribution of surface pathogens (P = 0.05). Highest hand contamination was Marco-Felipe King
predicted during Personal care despite the highest levels of hand hygiene. School of Civil Engineering, Pathogen Control
Ventilation rates of 6 ac/h vs. 4 ac/h showed only minor reductions in predicted Engineering Institute, University of Leeds, Leeds LS2
9JT, UK.
hand colonization. Pathogens accrued on hands decreased monotonically after
Tel.: +44 113 343 1957
patient care in single rooms due to the physical barrier of bioaerosol
Fax: +44 113 343 2265
transmission between rooms and subsequent hand sanitation. Conversely,
e-mail: m.f.king@leeds.ac.uk
contamination was predicted to increase during contact with patients in four-
bed rooms due to spatial spread of pathogens. Location of the infectious patient
with respect to ventilation played a key role in determining pathogen loadings Received for review 4 August 2014. Accepted for
(P = 0.05). publication 15 January 2015.

This is an open access article under the terms of the


Creative Commons Attribution License, which permits
use, distribution and reproduction in any medium, pro-
vided the original work is properly cited.

Practical Implications
We present the first quantitative model predicting the surface contacts by HCW and the subsequent accretion
of pathogenic material as they perform standard patient care. This model indicates that single rooms may sig-
nificantly reduce the risk of cross-contamination due to indirect infection transmission. Not all care types pose
the same risks to patients, and housekeeping performed by HCWs may be an important contribution in the
transmission of pathogens between patients. Ventilation rates and positioning of infectious patients within
four-bed rooms can mitigate the accretion of pathogens, whereby reducing the risk of missed hand hygiene
opportunities. The model provides a tool to quantitatively evaluate the influence of hospital room design on
infection risk.

ognition that the hospital environment plays an impor-


Introduction
tant role.
Risk of healthcare-acquired infections (HCAI) is Evidence suggests that at least 20% of HCAIs
omnipresent in healthcare facilities worldwide, and potentially could have arisen from an environmental
understanding transmission routes is key to effective reservoir (Harbarth et al., 2003) and several recent
control. While the transmission routes for some dis- studies have highlighted the importance of surface
eases are well documented, the precise mode of trans- contamination and indicated a causal link to subse-
mission is uncertain for many infections, particularly quent patient infection (Bhalla et al., 2004a). However,
for those pathogens that cause HCAI. Although it is there is currently little robust understanding as to how
probable that the majority of transmission occurs via a healthcare worker (HCW)–surface contacts and activi-
contact route (Sax et al., 2009), there is increasing rec- ties in the healthcare environment result in HCW or

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Modeling environmental contamination in hospital rooms

patient exposure to such pathogens. Studies of human and interaction with human behavior is still in its
behavior in the healthcare environment have largely infancy (Zartarian et al., 2012). Furthermore, the influ-
acknowledged the lack of a comprehensive survey ence of airflow patterns and ward design on the risk of
which collects the minutiae of hand-to-surface contacts this combined transmission route is not well under-
(Duckro et al., 2005; Pittet et al., 1999; Smith et al., stood. Single-bed rooms are widely advocated over
2012). Major studies have however, highlighted that four-bed patient environments for their infection con-
environmental contamination, through the deposition trol potential, yet there are little data to allow quantifi-
of bioaerosol on surfaces, cannot be underestimated in cation of the touted benefits (Ulrich and Zimring,
the contribution to fomite-based infection transmission 2008).
(Dancer, 2008; King et al., 2013; Otter et al., 2011; This research focuses on the combined interaction
Rusin et al., 2002). Surfaces such as bed rails have between deposition of airborne microorganisms, room
been linked with harboring microorganisms that cause design, and human behavior by considering the ques-
hospital infections, and many frequently used surfaces tion: Are single-bed patient rooms more effective than
in hospitals have been found to sustain viable patho- their four-bed counterparts at reducing the risk of
gens including staphylococci, enterococci (Duckro infection from environmental contamination? The
et al., 2005; Hayden et al., 2008; Pittet et al., 2006), study compares hospital single- and four-bed room
and Clostridium difficile (Roberts et al., 2008). In addi- environments by modeling likely contamination on the
tion, indirect infection transmission shows a distinct hands of healthcare workers resulting from pathogens
possibility of being exacerbated by incomplete or non- released from an aerosol source and deposited on sur-
existent surface cleaning (Bogusz et al., 2013). Patho- faces. The model combines computational fluid
gens have been also shown to accrue on HCW hands dynamics (CFD) simulations of room airflow and par-
as they touch surfaces (Pittet et al., 1999), and there is ticle deposition (King et al., 2013) data from HCW
evidence they can subsequently be transmitted to hand–surface contact patterns established through a
patients (Hayden et al., 2008). hospital observational study and a dermal pathogen
Hospital designs are tending toward incorporating accretion model to simulate contamination of HCW
single rooms, based on the premise that single room hands. The resulting probabilistic pathogen accretion
enables 24/7 admissions without disruption to other model (PAM) is used to compare the effect of room
patients, and the design will improve confidentiality for layout and ventilation rate on HCW hand contamina-
clinical discussion, examinations, and treatment tion during six different types of patient care.
(Chaudhury, 2005). In reviewing the literature, Chau-
dhury (2005) further report single rooms to promote a
therapeutic environment that is patient and family Methodology
centered increasing recovery and reducing infections
Patient rooms
and risks and enhancing the healthcare professional
and patient relationship. This evidence is supported by Two room scenarios are considered: a typical hospital
Ulrich and Zimring (2008), when considering the NHS single room and a standard four-bed room. Both room
Estates perspectives and further purport that single layouts are based on the UK Department of Health
rooms provide increased levels of protection and standard, HBN04-01(Department of Health Estates
prevention from infection. and Facilities Division, 2008), and computer aided
In addition, research has explored these issues in design models are illustrated in Figure 1.
depth, where there is an increasing body of evidence Rooms are assumed to be fully occupied, with one
which points toward a relationship between hospital infectious patient in each scenario. In both rooms,
room design and infection control (King et al., 2013; modeling is conducted with the ventilation at 6 air
Pittet et al., 2006; Shih et al., 2007; Tian et al., 2006). changes per hour (ac/h), as per the UK Department of
Ventilation is well recognized as a control strategy for Health guidance, HTM03-01 (Department of Health,
airborne infection (Zhang et al., 2009) and is recom- 2007) and at a reduced rate of 4 ac/h. In the case of the
mended for diseases such as tuberculosis, measles, four-bed ward (cases 3–10), the relative influence of
SARS, and more recently influenza (Yang et al., 2011). ventilation design was also considered through chang-
Aerial dispersion of bioaerosols has been associated ing the location of the infectious patient. All cases
with non-respiratory pathogens in hospitals including together with a brief description are shown in Table 1.
methicillin-resistant Staphylococcus aureus (MRSA)
(Sherertz et al., 1996) and C. difficile (Roberts et al.,
Environmental contamination
2008), and subsequent contamination of surfaces has
been recognized as a potential transmission route for Computational fluid dynamics (CFD) simulations were
some infections (Bhalla et al., 2004b). However, carried out to predict the likely spatial deposition pat-
research into the combined role of airborne dispersion, tern resulting from bioaerosols released from a quies-
pathogen contamination of hospital room surfaces, cent patient in the single- and four-bed room. The

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King et al.

(a) (b)

Single-bed room Four-bed room

Fig. 1 Typical room layouts from HBN04-01, as used in CFD simulations, showing simplified furniture arrangement, ceiling mounted
supply and wall mounted extract. (a) single room and (b) four bed room

Table 1 Case study scenarios been shown to heavily influence flow results (Roache,
1997); therefore, a mesh independence study was based
Case N° Room type Room dimensions ac/h Infectious patient on the formulation set out in King et al. (2013). For
1 Single-bed 4.7 9 3.8 9 2.8 m 4 Patient’s head this three hexahedral, grids with nominal cell sizes of
2 Single-bed 6 Patient’s head 50, 25, and 20 mm were compared. Velocity variation
3 Four-bed 6.8 9 7.6 9 2.8 m 4 Patient 1 was found to differ less than 5% between the 25 and
4 Four-bed 4 Patient 2 20 mm meshes at selected points within the bulk flow.
5 Four-bed 4 Patient 3
A maximum cell volume of 1.5625 9 105 m3 was
6 Four-bed 4 Patient 4
7 Four-bed 6 Patient 1 used within the bulk domain, and 1 9 106 m was
8 Four-bed 6 Patient 2 used 10 cm away from all horizontal surfaces. Final
9 Four-bed 6 Patient 3 cell count for all simulations was approximately 4 and
10 Four-bed 6 Patient 4 8 million volumes for the single- and four-bed rooms,
respectively.
Mechanical ventilation was modeled through a sim-
CFD methodology is detailed below and has previ- plified four-way ceiling supply diffuser (Zhang et al.,
ously been shown to compare well to experimental 2009) with velocity boundary conditions specified to
measurements of bioaerosol deposition in chamber give the air change rates in Table 1. Air was assumed
studies (King et al., 2013). In this previous study hospi- to be extracted via a wall-mounted grille, with a pres-
tal, single-bed and two-bed rooms were replicated sure boundary condition of 10 Pa. Turbulence was
inside an aerobiology chamber at the University of modeled with a Reynolds’ Stress (RSM) closure model
Leeds (4.2 93.2 9 2.2 m) with steady ventilation at 6 and standard wall functions; this model was shown in
ACH. Staphylococcus aureus was aerosolized by a Col- the previous study to compare better with experimental
lison Nebuliser (CN 25; BGI Inc., Waltham, MA, bioaerosol deposition data than the more commonly
USA) (mean diameter 2.5 lm) and released into the used k-epsilon model (King et al., 2013). Human
room for 30 min at the head of a supine heated manne- patients lying supine on the beds were represented
quin. Deposition of bacterial colonies was quantified through simplified blocks emitting a heat flux of
on key surfaces by means of nine agar-filled petri 56 W/m2. Air entering the room was at 20°C and all
dishes per surface CFD simulations conducted in Flu- walls were adiabatic. Bioaerosols were modeled using a
ent v.13 (ANSYS, Canonsburg, PA, USA) and follow- Lagrangian particle tracking method with discrete ran-
ing the methodology outlined below were used to dom walk. In each case, 10,000 2.5 lm diameter inert
model deposition of 2.5 lm particles released at the particles were released via a volume source located
same location and with the same geometry as the 10 cm above the patient’s head and given an inlet
experimental scenarios. Normalized concentrations on velocity of 1 m/s in the positive vertical direction to
surfaces were seen to compare well between the experi- represent exhalation.
ments and CFD model, giving confidence that the
CFD modeling approach can predict a realistic spatial Table 2 Surface categories and modeled surfaces in CFD geometries
deposition pattern in a ventilated room. Equipment Patient Near patient Far patient Hygiene areas
In the current study, steady-state airflow simulations
were carried out using Fluent v.13 (ANSYS) for the Location on bed wall Mannequin Bed Window Sink
model hospital room geometries shown in Figure 1. (1 9 0.4 m) Chair Workstation Towel dispenser
Tray
Meshing, carried out in ANSYS Workbench v13, was
Bedside table
fully hexahedral. Grid density and construction has

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Modeling environmental contamination in hospital rooms

Nine surfaces of interest were defined within the with which they happened were recorded. Typical loca-
CFD model, as indicated in Table 2, and the modeled tions of these surfaces are shown in Figure 2. The
particle concentration was determined on the surfaces occurrence and type of hand hygiene after each care
for each scenario in Table 1. These surfaces were based episode was also recorded. Over 400 individual care
on those monitored during the observation study out- episodes were observed.
lined below. Data from the observations were used to generate
CFD simulations were carried out on a University representative contact patterns to model the likely
of Leeds’ high-performance facility (ARC1 with 672 sequence of surface contacts by a HCW in a patient
AMD cores and 128 GB memory), were considered room. HCW were found to touch surfaces in a non-ran-
converged when residuals for continuity and all other dom sequential or directed manner, insofar that mov-
variables dropped below 1 9 104, and remained ing from one surface category to another has a higher
below this for at least 100 iterations. All variables probability than a transition to somewhere else. By
are scaled with respect to the sum of the errors in all assigning each surface category a numerical value from
cells. In addition, continuity is scaled with respect to 1 to 5, where Equipment = 1, Patient = 2, Hygiene
the largest absolute value within the first five itera- areas = 3, Near-bed surfaces = 4, and Far-bed sur-
tions and so can be considered normalized (ANSYS faces = 5, the movement of the HCW between surfaces
2010). can be represented by means of a weighted probability.
The movement of HCW between surfaces is modeled
using a Markov chain approach (Allen, 2008). Using
HCW–surface contacts
the defined weighted probabilities, the movement of a
The likelihood of healthcare workers having contact HCW between surfaces can be simulated based on the
with surfaces during patient care was developed from property that, given the present state, the future and
surface contact data accrued during an observational past states are independent. This is termed the Markov
study carried out at a National Health Service (NHS) Property:
single-bed accommodation hospital ward during the
first quarter of 2012. Healthcare workers were PðXi ¼ xi jXj ¼ xj Þ: ð1Þ
observed during episodes of care categorized into six
areas described in Table 3, following standardized cat- Given the five surface categories, the probabilities
egories set out in Pittet et al. (1999) and Dancer et al. can be expressed in a transition matrix (P) indicating
(2010). the maximum likelihood of directed contact between
In each observed care episode, hand-to-surface con- any pair of surfaces. For example, if the HCW is cur-
tacts with surfaces set out in Table 4 and the sequence rently touching surface category 1, p12 is the probabil-
ity that they will then touch surface category 2. This
Table 3 Six care types with examples of procedures within each type
probability is derived from the observed data by count-
ing the occurrences of the transition 1?2 for each
Medication Personal HCW in the observational study and dividing by the
Direct care Housekeeping Mealtimes rounds Miscellaneous carea
total number of surface transitions throughout their
episode of care. Thus, Pbij ¼ P ij , where m = 1. . .5
x
Blood pressure Equipment Distribution Distributing Call bell Toileting
measurement cleaning of meals medication request m
xik
Weighing Cleaning Injections Response to Patient states, and indices i, j, and k are dummy indices to indi-
patients patient pressure changing
cate summation.
surfaces mattress
alarms The observed data enabled surface contact transition
Blood sugar matrices to be created for single-patient rooms, but to
saturation compare single- and four-bed rooms, HCW behavior
a in the four-bed room must be modeled. This was
Note that limited observations were made for personal care episodes for patient privacy
reasons. undertaken by assuming that care approaches were
similar in the two room types and adjusting the transi-
Table 4 Surfaces within each surface category during the monitoring study tion probabilities based on other published informa-
tion. Smith et al. (2012) conducted an observational
Surface category
study of HCWs in a four-bed room applying the same
Equipment Patient Near patient Far patient Hygiene areas surface category criteria as used here. However, they
note that patient charts become near-bed objects as
IV stand Clothing Bedrail Window Alcohol gel
Hoist Bedding Curtain Soap dispenser
these are often at the foot of the patient’s bed rather
BP cuff/stand Tray Light switch Tap the far side of the room; in our single-bed rooms, chart
Notes trolley TV Chart Sink positions were modeled as a far-bed surfaces as the
Medication trolley Chair Door/handles Paper towel dispenser chart was located on the workstation (Figure 2) in the
Bedside table observation study. Therefore, this adjustment is made

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King et al.

(a) (b)

Surfaces around the bed Surfaces far from the bed

Fig. 2 Typical location of surfaces in the single room which were monitored for HCW contacts. (a) room surfaces close to the bed and
(b) surfaces close to the door

to the probability densities derived from the healthcare proportional to the amount released initially in each
observations. A Wilcoxon rank-sum nonparametric case. The parameter V is regarded as the initial condi-
test comparing Smith et al.’s (2012) data to the current tion for the PAM model simulations, with the surfaces
study shows that no statistical difference exists at the already contaminated at the point the HCW is
5% level (P = 0.068), highlighting that the only differ- assumed to enter the room. In addition, if each particle
ence in HCW behavior between single- and four-bed is treated as one cfu, the resulting deposition in cfu/cm2
rooms is the positioning of patient charts. Conse- is comparable to actual hospital values (Mulvey et al.,
quently, this demonstrates the similarity between nurse 2011).
behavior in single- and four-bed rooms. All four-bed
simulations use this adjusted behavior in line with Hand–surface contact area, A (cm2). This is assumed to
Smith et al. (2012). exhibit a continuous distribution based on experimen-
tal values from Brouwer et al. (1999). They show that
this can be modeled as a lognormal distribution with
Pathogen accretion model
an arithmetic mean of 7 cm2 and standard deviation of
Colonization of HCW’s hands through contact with a 1.9 cm2 [corresponding to lnN~(0.84,1.3)]. For each
contaminated surface is considered to be a dynamic surface contact, it is assumed that either hand may be
process in which multiple factors may vary. The num- in contact with the surface and no distinction is made
ber of microorganism colony forming units, Y (cfu), for right- or left-handedness.
accrued on HCWs hands from environmental or
patient surface contacts during patient care can be Surface-to-Hand Transfer efficiency, k. It is reasonable
shown via sensitivity analysis to depend primarily on to assume that not all of the pathogens in contact with
six variables (Pessoa-Silva et al., 2004). the area of skin touching the surface are transferred to
the hands. Transfer efficiency, which represents the
Y ¼ Yðn; A; V; k; b; hÞ: ð2Þ percentage of surface contaminant transferred to the
hand during a contact event, has been shown to be one
The number of surfaces touched, n. Each type of care of the most important parameters when modeling der-
shows a variable pattern of surface contact frequencies mal exposure (Xue et al., 2006). Unfortunately, it is
and sequences. Probabilistic distributions for these one of the most troublesome to accurately measure
were obtained from the observational study as outlined (Beamer et al., 2009). Transfer efficiency could be a
above. function of multiple ambient parameters such as sur-
face physiology, contact frequency, duration and pres-
Surface contamination, V (cfu/cm2). The concentration sure, concentration of transferrable material on
present on each room surface is dependent on the sce- surface, temperature, and humidity. Rusin et al. (2002)
nario in question. These are obtained from sampling conclude from experimental studies that the transfer
the lognormal distribution based on the CFD simula- efficiency from surfaces to hands also varies between
tions for each scenario, as described above. It must be microorganism species. In three separate experiments,
highlighted that this study considers no microbial they reported the transfer of Gram-positive bacteria,
die-off due to environmental stress as this is a time- Gram-negative bacteria, and bacteriophage to be
dependent phenomenon. Therefore, V is assumed to be 38.5%, 65.8%, and 27.6–40%, respectively, from

698
Modeling environmental contamination in hospital rooms

60 ence on hand hygiene efficacy, which is likely to be due


to their individual adherence properties (Boks et al.,
50 2008). Particular difference is noticed between bacteria
and viruses (or bacteriophage), where removal of the
latter is often an order of magnitude lower. Neverthe-
40
less, bacteria have the primary concern of many infec-
Transfer %

tion control teams, where MRSA or C. difficile often


30 rank highest on the prevention list. Consequently, the
model is non-organism specific, whereby resident or
20 background microflora is ignored. Whether or not
hand antisepsis actually occurs following an episode of
10
patient care is based on the probabilities derived from
the observation study and depends on care type.
Following a variance based sensitivity analysis using
0
Non-porous Porous total effect Sobol indices (Nossent et al., 2011), the
function shown in Equation 2 can be used to model
Fig. 3 Surface-to-hand transfer efficiency (k). Data derived from pathogen accretion (Y) by means of a recurrence rela-
Rusin et al. (2002)
tionship given in Equation 3. This represents the hand
pathogen loading at any time-step after contact with
non-porous surfaces. However, they indicate the trans- any one surface.
fer rate reduces to below 10% when porous fomites are
evaluated. As there are insufficient data available in the Yi ¼ ki Vi Ai þ bi Yi1 ; ð3Þ
literature to model the influence of specific parameters,
the model employs the distribution developed by Rusin where i = 1. . .n is the surface contact count. For pur-
et al. (2002), as shown in Figure 3, to represent the poses of remaining succinct, let r = kAV then assum-
variability in transfer efficiency. ing that the transfer of pathogens to the surface from
the HCW occurs sequentially and is independent of the
Hand-to-surface transfer efficiency, B. A significant surface loading then Y can be described as follows:
quantity of material residing on hands may also be
transmitted to the surface during contact (Otter et al., Yi ¼ ri þ bi  ðri1 þ bi  ðri2 þ   ÞÞ
2013). Montville and Schaffner (2003) demonstrate ¼ ri þ bi ri1 þ bi bi1 ri2 þ   
that a difference exists between the direction of trans- ! ð4Þ
fer, with statistically significantly lower transmission Xi Y i

shown during transfer from hands to fomites than vice ¼ bk rj :


j¼0 k¼jþ1
versa. They also highlight the influence of inoculum
size on the efficiency of transfer, showing that when
HCW touching surfaces during an episode of
high levels are used, transfer rates are more accurately
patient care forms the driving force within this model.
characterized (Montville and Schaffner, 2011). Surface-
The model was programed using Matlab (Math-
to-hand transfer efficiencies (b) are sampled from
Works, Natick, MA, USA). For each scenario, a
Monteville et al.’s empirical data. Therefore, during
Monte Carlo simulation of 1,000 HCW care episodes
hand-to-surface contact, a proportion of pathogens
was conducted for each care type, modeling the
already acquired by the HCW may be deposited from
mechanics of pathogen transfer based on the input
the hand onto the surface (Rusin et al., 2002). Random
parameters set out above.
sampling is conducted from data in Montville and
Schaffner (2003).

Antisepsis efficacy, h (%). This refers to the efficiency Results and discussion
of reducing microbial contamination of HCWs’ hands
Bioaerosol deposition
after performing one of three types of hand hygiene:
hand washing with either bland or medicated/antibac- Surface deposition concentrations, cfu/cm2 predicted
terial soap, removal of non-surgical gloves, or dry rub- from the CFD simulations following the release of
bing with a waterless alcohol agent (minimum 61% 10,000 cfu, can be seen in Figure 4. These show the
ethanol by volume). Here, hand hygiene efficacy is breakdown of particle concentration for the five differ-
based on data from published studies where significant ent surface categories and, in the four-bed case, for
sample sizes are available (Girou et al., 2002; Montville each infectious patient position in turn (Figure 4b–e).
and Schaffner, 2003; Sickbert-Bennett et al., 2005). Deposition in the single room (Figure 4a) appears to
Microorganism type has been shown to exert a differ- be mainly focused on the equipment area and the

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King et al.

(a)

(b) (c)

(d) (e)

Fig. 4 Predicted particle deposition (cfu/cm2) on horizontal surfaces within the single- and four-bed accommodation for an initial
release of 10,000 cfu. Comparison shown between 4 ac/h and 6 ac/h for each case. (a) case 1 & 2 in the single room, (b) cases 3 & 7 in
the four-bed room where the infectious patient is in position 1, (c) cases 4 & 8 in the four-bed room where the infectious patient is in
position 2, (d) cases 5 & 9 in the four-bed room where the infectious patient is in position 3 and (e) cases 6 & 10 in the four-bed room
where the infectious patient is in position 4. E = Equipment, P = Patient, H = Hygiene areas, N = Near-patient surfaces, F = Far-
patient surfaces

patient themselves, and the model predicts little differ- and 4. Equally when patient 3 is the source (Figure 4d),
ence in the deposition pattern between 4 and 6 ac/h. In negligible counts can be found in the vicinity of patient
the case of the four-bed room, predicted surface con- 1 or patient 2, and when patient 4, closest to the
centrations are highest in the vicinity of the source extract, is the source, there are very few counts in the
patient in all cases. Surfaces opposite the source posi- vicinity of any of the other patients. However, the
tion demonstrate a sharp drop-off; here, particles distribution when patient 1 is the source (Figure 4b) is
appeared to be maintained airborne and directed noticeably different with deposition predicted across
toward the extract. This is particularly the case when the room.
patient 2 is the source (Figure 4c), where a seemingly Wong et al. (2010) suggest that as the air change rate
dichotomous partition within the room can be increases, the deposition increases further from the
observed, and few particles are deposited on patients 3 source. A one-way nonparametric Wilcoxon signed-rank

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Modeling environmental contamination in hospital rooms

Fig. 5 Mean and standard deviation of surface contacts observed and used in the model

Table 5 Transition matrices Pbij , showing directed probabilities of moving from surface i to surface j for each type of care

(a) (b) (c)

(d) (e) (f)

test does not uphold this conclusion here, and there is HCW during an episode of care in a single room by
no clear difference between the two air change rates. means of a stochastic simulation.
However, a statistically significant difference is exhib-
ited in the four-bed room (P = 0.04) between surface
Hand hygiene
concentrations for different infectious patients at the
same air change rates. The observational study data showed statistically sig-
nificant differences in hand antisepsis choice between
care types (P < 0.001), with some variation within
Surface contact sequences
each care type, as shown in Figure 6. Alcohol rub was
Observational study data indicated the probability of used abundantly throughout all but personal care,
contact with different surface categories (P = 0.04) where hand washing with soap and water predomi-
along with hand hygiene method (P = 0.02) was depen- nated. Glove usage accounted for only 2% of observed
dant on care type. Statistical differences were also sig- episodes of care, half of which were during housekeep-
nificant between the total number of surface contacts ing. These probabilities are incorporated into the PAM
and the likelihood of hand hygiene being performed for model to account for the likelihood of HCWs under-
different care types. It should be noted that this is not taking some form of antisepsis after each episode of
analogous to hand hygiene compliance as the research care (Figure 7).
team are not able to pass judgment on what hygiene
procedures should be followed for a particular care epi-
Model validation
sode. Figure 5 shows the mean and standard deviation
of surface contacts observed and used in the model: Published data which measures contamination levels of
cij for all care types
Table 5 shows transition matrices P HCWs’ hands are scarce. In particular, Pittet et al.
derived from all observed HCW surface–contact (1999) is the only known published study that quanti-
sequences. Briefly recapping, the transition states are as fies both cfu values along with the time spent in the
follows: 1 = Equipment, 2 = Patient, 3 = Hygiene room by the HCW. However, their methodology does
areas, 4 = Near-bed surfaces, and 5 = Far-bed surfaces. not include surface swabbing and hence a specific value
Using these directed probabilities, Figure 6 shows a for surface contamination, V, is not known. Neverthe-
typical example sequence of surface contacts by a less, assuming that other variables such as HCW hand

701
King et al.

Good comparison is shown particularly at lower (first


quartile) values (P = 1 9 103), where a higher con-
centration of data exists. Both lower-mid and upper-
mid quartiles compare well (P = 0.01 and P = 0.04).
Higher values of cfus (upper quartile) become less fre-
quent and the comparison is poorer (P = 0.12). The
reader must note that detection levels by glove juice
methods and subsequent culture techniques carried out
by Pittet et al. (1999) have led to truncated data, which
is likely the reason for less optimal comparison at this
level. If these data were extrapolated, PAM potentially
may approximate the behavior better in the upper
quartiles (P ~ 0.02). However, pending greater sources
of data, it is not unreasonable to conclude that at least
through the first two quartiles or the first 50% of cfu
colonization levels, PAM is a capable and realistic
Fig. 6 Example of surface contacts of HCW #50 performing an model.
episode of direct care

Application of PAM to single- and four-bed rooms


surface area, surface types, and nursing behavior are Air change rate. Results from PAM are all normalized
comparable between scenarios, it is reasonable to com- with respect to the mean contamination level on
pare the distribution shape by means of a Kendall-tau HCWs’ hands after direct care in the single room at
nonparametric test of the simulated cfu from PAM 6 ac/h. This can be considered the ‘base case’ and
and the measured data by Pittet et al. (1999). Specifi- enables comparison between rooms, ventilation, and
cally, this is a measure of rank correlation or the simi- care types.
larity of the orderings of the data when ranked by each Figure 8 depicts predicted normalized cfu on HCW
of the quantities. This approach is used for comparing hands, Y, compared against the average of direct care
the differences between individual observations with for each subsequent type of care within the single
respect to each other to gain an insight into the overall room. Additionally, the comparison is made between a
data distribution. ventilation rate of 4 and 6 ac/h. Initially, there appears
Initial comparison shows a less-than-perfect fit only to be a small reduction in hand contamination
(P ~ 0.2), and therefore, the data from both PAM from 4 to 6 ac/h when comparing medians, and com-
and Pittet et al. were split into 4 groups corre- parison of the upper quartile shows small differences
sponding to: lower quartile (≤25%), lower-mid depending on care type. However, comparison of
quartile (25% < x ≤ 50%), upper-mid-quartile (50% extrema using a Kruskal–Wallis nonparametric test
< x ≤ 75%), and upper quartile (75% < x ≤ 100%). reveals that predicted hand contamination levels under

Fig. 7 Cumulative probability of hand hygiene category subdivided by care type

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Modeling environmental contamination in hospital rooms

Fig. 8 Boxplots showing predicted normalized cfu values on HCW hands for a single room before hand hygiene, comparing 4 and
6 ac/h

(a) (b)

(c) (d)

(e) (f)

(g) (h)

Fig. 9 HCW route for all care types in the single- and multi-bed rooms at 6 ac/h (a, b). Boxplots (outliers omitted) of cumulative nor-
malized Y values after different episodes of care (c–h). Multi-bed plots are an average of four episodes of care, varying the infectious
patient location

703
King et al.

a ventilation rate of 4 ac/h are consistently higher tious source. Here, we used a normalization metric to
throughout (P < 0.05). consider the relative spatial deposition. It is also
important to note that the CFD simulations were
Room type. In Figure 9, we consider two design steady-state models of the airflow that did not account
options: four patients located in four single rooms or for movement of people and only considered the depo-
colocated in one-four-bed room. In each case, the sim- sition of small (2.5 lm) diameter particles. We made
ulation assumes that one patient is infectious and that these assumptions here based on validation experi-
the HCW provides care to all four patients in turn. The ments for the CFD models (King et al., 2013). In real-
model assumes the worst case scenario where the first ity, infectious particles will be released in a size
patient attended to is the infectious one (Figure 9a,b). distribution that will include smaller and larger parti-
All other parameters in the model, including hand cles which will change the spatial deposition patterns;
washing are as set out in the methodology. Figure 9c– larger particles are likely to increase deposition close to
h shows the normalized contamination on HCW hands the patient. A CFD model incorporating a polydis-
(Y values) for progression through the series of four perse particle release based on known particle size data
patients in single- and four-bed rooms with no air- from respiratory (Han et al., 2013; Xie, 2008) and envi-
borne cross-transmission between the rooms. The ronmental (Hathway et al., 2013) sources could enable
results show that cfu values are likely to be monotoni- an estimation of the resulting spatial contamination,
cally decreasing as the HCW progresses between which can then be applied in PAM. However, without
patients in the single rooms. Environmental contami- experimental validation of the CFD model, these
nation due to the patient is only present in room 1, and results would have to be treated with caution.
hand antisepsis removes contamination in the majority Ventilation method and transient flows due to activ-
of cases and minimizes further environmental contami- ity are also factors. Under the HTM 03-01UK guid-
nation in subsequent rooms. In the case of the multi- ance (Department of Health, 2007), minimum air
bed room, the results are quite different. Rather than change rates of 6ACH are specified, but how and if
an expected decrease due to hand hygiene, the aerial these are achieved can vary. Hospital ventilation strate-
spread of microorganisms to neighboring bed bays gies in the UK often incorporate both natural and
allows for subsequent accretion of pathogenic material mechanical ventilation methods. While verification of
by the HCW regardless of hand hygiene. This accretion mechanical flow rates is largely feasible, in naturally
is also likely to happen without the HCW awareness; ventilated environments, measurement is more chal-
they may take additional precautions if they know that lenging. Although the small number of studies
patient 1 is infectious, but are not likely to modify care (Escombe et al. 2007, Qian et al. 2010, Gilkeson et al.
for other patients in the same way. 2013) suggest that high ventilation rates are achievable,
these may not have predominant or established airflow
pathways in some cases. When combined with activity
Discussion
such as human movement, opening and closing doors,
The study conducted here demonstrates the potential changes in buoyancy due to heat sources, and use of
for quantifying the effect of room design on potential fans for comfort, these variations in airflow patterns
infection risk by means of an indirect metric, namely may change the dispersion of airborne microorganisms
hand contamination. and further confound surface contamination patterns.
An observation and sampling study conducted on a
multi-bed respiratory ward (Hathway et al., 2013)
Bioaerosol deposition patterns
found that airborne microorganisms and particles var-
CFD modeling of the application scenarios revealed ied with the different activities on a ward, with
that a ventilation rate of 6 ac/h showed little significant increases during healthcare worker activity and per-
improvement over 4 ac/h on deposition quantities or sonal care, but little change with visitors on the ward.
spatial variation in three of the four considered scenar- Nevertheless, the approach presented here gives a real-
ios in the four-bed room. A decrease in spread locus istic mechanism for exploring potential deposition at
was noticed particularly when the infectious patient design stage and identifying design options that are
was placed closest to the outlet vent, highlighting the likely to minimize contamination.
greater downward momentum on particles exerted by
comparatively higher local air velocities at 6 ac/h. This
Observational study
indicates that both the ventilation diffuser locations
and ventilation rate may be important in influencing The first hand data accrued from the observational
deposition as well as extraction of airborne microor- study is of fundamental importance for the modeling
ganisms. It is recognized that exact cfu/cm2 values can- of human hand-to-surface contact events, allowing
not be obtained via this method due to the absence of insight into the different types of care and how these
knowledge regarding the concentration of the infec- also the behavior of nurses and doctors. These data

704
Modeling environmental contamination in hospital rooms

then formed the basis of a stochastic model of HCW acknowledged that full validation of the model is very
behavior as they moved from one surface to another challenging as the microbiome, ventilation design,
and consequently forms the driving force behind the physical layout, and personnel variation of every hos-
subsequent model for pathogen accretion. While the pital is highly specific. Data for the surface contamina-
data are only from one hospital with a single-bed ward tion patterns and the HCW hand–surface contact
environment, comparison with other studies suggests patterns were derived from CFD models and the obser-
the data are realistic and representative of typical vational study, respectively, as part of the study. While
health care in other hospital environments. However, it this leads to a reasonable degree of confidence in these
should be acknowledged that in applying the model to data in the particular scenarios examined, both param-
other hospital wards, it may be necessary to make eters are influenced by a number of factors as outlined
adjustments to the location of surfaces and contact above. The other model elements relied on published
patterns. For example, in the current study, the posi- data to provide suitable inputs. As far as possible,
tion of the patient charts and information in the single these were applied as distribution functions to account
rooms was treated as a far-bed surface based on the for variability; however, the influence of factors such
practice in the observation study, while in the four-bed as temperature, humidity, and surface porosity are not
room, it was treated as near-bed based on Smith explicitly considered in the model and cannot be deter-
et al.(2012). In other hospitals, the position of charts mined from the current results. With further data, it
may vary depending on room design, local practices, may be possible to include these factors, for example,
and care needs. Similarly, in wards where care routines into the transfer efficiency parameters.
differ substantially from those considered here, it may It should also be emphasized that the current model
be necessary to conduct a further observational study does not simulate the pathogen accretion process over
to create new hand-to-surface contact patterns that are a particular time period. The CFD deposition pattern
more representative of the environment. is used to generate a likely surface contamination pat-
tern for a given room, and the PAM then simulates the
contact sequence and likely resulting accretion. The
Probabilistic model
resulting hand contamination is presented in the study
The pathogen accretion model (PAM) was developed as a normalized parameter to enable relative compari-
from the growing understanding of hand contamina- son between scenarios, as the model does not include
tion from surface contacts. This model focuses on the transient factors that may influence the actual micro-
physical process of accruing pathogens onto either the bial concentration on HCW hands. In reality, micro-
skin or gloved surfaces of HCWs’ hands as they per- bial viability on surfaces and on hands will be a factor,
form episodes of standard patient care. The model pro- and this is influenced by temperature and humidity as
vides a framework which allows for the quantitative well as surface properties. Hand hygiene may also
comparison of hospital room design including single- influence microbial viability; alcohol gels are known to
vs. four-bed accommodation by means of HCW hand exert residual microbiocidal effects due to remaining
contamination. Application of PAM to the scenario residue on HCWs’ hands (Bogusz et al., 2013) which
rooms showed that differences were not clear cut and would also influence the actual microbial concentra-
the positioning of the infectious patient had most effect tions. The aerosol release of microorganisms will also
on the final results. The spatial deposition of particles be a continuous and transient process, with surfaces
is influenced by the location of the ventilation supply never having a steady-state concentration due to ongo-
inlet relative to the source. Locating a susceptible ing deposition interspersed with cleaning activities.
patient closer to the supply air is likely to reduce the Although this means that the model cannot explicitly
risk of environmental contamination due to bioaerosol model infection risk, the current formulation enables
release from a neighboring patient. Locating the infec- exploration of the likely importance of different design
tious patient in a four-bed room without an unob- and care factors and incorporates the combined effects
structed air pathway from the bed to the ventilation of airflows and human activities. In particular, it
outlet caused the highest level of surface contamination enables direct and quantitative comparison between
of all scenarios tested. These findings concur with different ward designs under the same care conditions.
experiments and simulations conducted in King et al. The framework also allows for increasingly precise
(2013). specification of surface contamination levels, transfer
It is crucial to highlight that this is a flexible frame- parameters, and HCW contact patterns with input of
work model, built from the increasing understanding further data from sampling and observation studies.
of the mechanics behind pathogen transmission; how-
ever, the results are dependent on several data inputs
Conclusions
to the model which all have a degree of uncertainty.
Initial validation was successful against the limited The aim of this study was to provide a mathematical
available data in the published literature, but it is model which quantifies the relative contamination

705
King et al.

levels of healthcare workers’ hands from surfaces The results support the hypothesis that single-patient
within hospital rooms. This is achieved through a mul- rooms reduce the risk of HCAI, highlighting that
tidisciplinary approach coupling CFD simulations with this benefit may extend to risk of infection due to
clinical observation of HCW movement and Markov environmental contamination not just the more obvi-
chain Monte Carlo modeling of hand contamination. ous airborne and direct contact transmission routes.
An observational study of patient care in a single-bed The findings also suggest that ventilation design and
hospital ward showed that hand hygiene choice and room layout may affect environmental contamination
frequency varied strongly. HCWs performing short and subsequent contact transmission risks in multi-bed
episodes of care had a predilection for alcohol rub. In environments. This has implications for those design-
other care types, the usage of alcohol rub or soap and ing wards as well as operational aspects in terms of the
water was 50/50. HCW surface contact patterns in most suitable location for infectious or susceptible
rooms were modeled by a Markov chain and fed into a patients.
mathematical model to calculate the pathogen coloni- This study makes a significant contribution to the
zation level on hands after patient care. body of evidence that support the NHS in making deci-
A parametric study indicates that hand contamina- sions about hospital design and whether or not to
tion levels depend highly on care type (P < 0.0001), incorporate single rooms.
the number of surface contacts (P < 0.001), and the
distribution of surface pathogens (P = 0.05). Highest
Acknowledgements
hand contamination was predicted during Personal
care despite this having the highest levels of hand This work was carried out as part of a PhD studentship
hygiene. This is due to the greater number of contacts supported by the UK Engineering and Physical Sci-
on the more highly contaminated near-bed surfaces. ences Research Council (EPSRC), EP/G029768/1 and
Increasing the ventilation rate is likely to have a small Arup. The observational study was approved by the
benefit on environmental contamination in a single- South East Wales Research Ethics Committee (11/
bed room, while the relative location of infectious WA/0200). The authors would like to thank Sue Bale,
patients and ventilation supply and extract grilles had Liz Waters for valuable input into the preparation of
a significant effect in a four-bed room (P = 0.05). Com- this manuscript and all the staff at the Ysbyty Aneurin
parison of four patients housed in single rooms against Bevan for facilitating the observational study.
a four-bed room suggests contamination on the
HCWs’ hands is likely to decrease monotonically after
Conflict of interests
care in single rooms, but is likely to increase during
contact with subsequent patients in four-bed rooms. None to report.

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