Transmission of communicable respiratory infections and facemasks
Journal of Multidisciplinary Healthcare
Transmission of communicable respiratory infections and facemasks
Yi Li 2
Yue Ping Guo 2
Kwok Ching Thomas Wong 1
Wai Yee Joanne Chung 1
Mayur Danny Indulal Gohel 0
Hang Mei Polly Leung 0
0 Department of Health Technology and Informatics, The Hong Kong Polytechnic University , Hung Hom, Kowloon, Hong Kong SAR , China
1 School of Nursing
2 Institute of Textiles and Clothing
Background: Respiratory protection efficiency of facemasks is critically important in the battle against communicable respiratory infections such as influenza and severe acute respiratory syndrome (SARS). We studied the spatial distributions of simulated virus-laden respiratory droplets when human subjects wore facemasks and were exposed to regulatory viral droplets by conducting in vivo experiments in facemask use. Methods: Transmission pathway of aerosols of Fluorescein-KCl solution through facemasks and protective efficiency of facemasks were examined by using normal surgical facemasks and two facemasks with exhaust valves (Facemask A) and exhaust holes (Facemask B) covered with the same surgical filters situated at the back of the facemasks. Fluorescein-KCl solution was sprayed onto the faces of participants wearing the facemasks and performing intermittent exercises on a treadmill in a climatic chamber. Results: Experimental results showed that when droplets spread onto a person face-to-face over short distances, 92.3% to 99.5% of droplets were blocked by the front surface of the facemask, whereas only 0.5% to 7.7% of droplets reached the back of the facemask. Both facemasks A and B had near or over 99% protection efficiency, compared with that of 95.5% to 97% of surgical facemasks. Using the same filters as normal surgical masks, facemasks A and B provided more effective respiratory protection against communicable respiratory infections such as influenza and SARS by the location of the breathing pathway to the back of the facemasks. Conclusions: Separating the breathing pathway from the virus-contaminated area in facemasks can provide more effective protection against communicable respiratory infections such as influenza and SARS.
An influenza pandemic has the potential to cause more death and illness than any other
public health threat
. Since January 2004, a total of 240 human cases
of avian influenza A (H5N1) have been reported to the World Health Organization
(WHO) and of these cases, 141 were killed by H5N1
pointed out that the greatest concern is that human-to-human transmission may
begin if there is a change in the vital genome of avian influenza.
The main way that influenza viruses are spread is from person to person via
virus-laden respiratory droplets (particles with size ranging from 0.1 to 100 µm in
diameter) that are generated when infected persons cough or sneeze
(Roy and Milton
2004; CDC 2006)
. These respiratory droplets can then be directly deposited onto the
mucosal surfaces of the upper respiratory tract of susceptible persons who are near
(ie, within 3 feet) the droplet source such as healthcare workers (HCWs) in healthcare
environments. Therefore, it is recommended that healthcare personnel use a fit-tested
respirator, at least as protective as a National Institute for Occupational Safety and
Health (NIOSH)-approved N95 filtering respirator for close patient contact with known
or suspected avian influenza to decrease transmission of
influenza in healthcare settings (CDC 2005).
The efficiencies of single-use facemasks were studied
by a number of research groups in laboratory settings
et al 1994; Willeke et al 1996; Qian et al 1998)
. Willeke and
colleagues (1996) reported that the mean efficiencies of a
surgical facemask was 97% and found that spherical corn oil
particles and spherical bacteria have the same penetration in
size range from 0.9 to 1.7 µm for surgical facemasks. Qian
and colleagues (1998) reported that N95 respirators provide
excellent protection against airborne particles when there is
a good face seal. The filtration efficiency of unloaded N95
mask is 99.5% or higher for particles larger than 0.75 µm and
95% or higher for the most penetrating particle size of about
0.1 to 0.3 µm. However,
Martyny and colleagues (2002
reviewed respiratory protection and found that respirators
can save lives, but cannot guarantee complete protection.
Bałazy and colleagues (2006
) reported that the penetration
of virions (particle size range of 0.01–0.08 µm) through N95
respirators can exceed an expected level of 5%. The influenza
virus is a globular particle with about 0.08–0.12 µm in
(Mandell et al 1995)
. Therefore, viruses may be able to
penetrate or spread through N95 respirators.
pointed out that some
HCWs were infected with SARS despite wearing full
personal protective equipment (PPE; gloves, gown, and
N95 respirators). An intensivist who wore full PPE
including a N95 respirator became infected with SARS during a
bronchoscopy at a Singapore university hospital
. A physician who cared for the wife of the initial case
patient in Taiwan developed clinical features that met the
criteria for a probable SARS case and was confirmed to
be infected with the SARS coronavirus by the laboratory. He
was considered as being infected by a direct line of droplet
spread when the SARS patient had episodes of coughing
while sometimes partially sitting up during the performance
of a chest ultrasound and while supervising the intubation
despite using a N95 respirator
(Twu et al 2003)
. Moreover, 5
patients with SARS in a teaching hospital in Singapore were
HCWs who had contact with patients although they wore PPE
(Ho et al 2004)
. Therefore, Tambyah (2004) concluded that
PPE is effective most of the time, but sometimes additional
protection is needed. Undoubtedly, the issues demand further
investigation. There is a strong need to explore the reasons
that commercially available respirators cannot guarantee
complete protection from the mode of transmission of
virus-laden respiratory droplets. The protective principles
of a typical filtering facemask must be studied to guide the
design and use of facemasks for enhancing their protective
Figure 1A shows the possible pathway of contaminated
droplets spreading from an infected person onto the face of a
susceptible host. When an infected human coughs or sneezes,
particles of varying sizes ranging from large particle droplets
(about 100 µm in diameter) to small particle droplets (about
0.1 µm in diameter) are created. These droplets could reach
the alveolus of a susceptible host when respiratory
protection is not employed. When the susceptible person wears a
respirator in a face-to-face position, most of the contaminated
droplets spreading onto the person’s face from infected
person were blocked by the front surfaces of the respirator.
Figure 1B shows that when the droplets contaminated with
influenza viruses (about 0.08–0.12 µm in diameter) reach the
front surface of a facemask, they can stick to the surfaces that
have pore sizes from 0.3∼50 µm in diameter if a facemask
is not strongly water-repellent or can be absorbed by the
facemask if the facemask is water-absorbent particularly
since the expired air would most likely wet the facemask
(Li and Li 2005)
Figure 2 shows the structure of the commonly used
facemasks and the possible transmission pathway of virus when
a typical filtering facemask is worn. As Figure 2A shows,
virus-laden respiratory droplets could spread onto whole
face of a susceptible host and form a virus-contaminated
area inside an imaginary frame. A typical filtering facemask
mainly protects the parts of the face under the wearer’s eyes
under an imaginary horizontal line (Figure 2B). Its filter
ventilates air and obstructs viruses, and the filter of a typical
filtering facemask becomes accordingly both breathing and
filtering areas. It is clear that the virus-contaminated area
overlaps over the filtering-breathing area on the filter of a
typical filtering facemask (Figure 2C). Consequently, inhaled
air could be contaminated when wearers exhale and inhale
during breathing cycles through the filter of a typical filtering
facemask (Figure 2D). This mode of transmission of
virusladen respiratory droplets on facemasks and the structure
of a typical filtering facemask might be responsible for the
incomplete protection of commercially available facemasks
in some healthcare occasions.
On the basis of the mode of droplet transmission and
the protective principle of a typical filtering facemask, we
assume that separation of the breathing pathways from the
virus-contaminated areas could minimize the contamination
of inhaled air. Figure 3 illustrates this hypothesis using
two newly designed facemasks with exhaust valves/holes
at the back of facemask, in which the front surface of
facemask obstructs viruses and becomes accordingly a
virus-contaminated area. The breathing channels, ie, exhaust
valves/holes, are placed at the back of facemask far from
the virus-contaminated areas. The breathing channels are
covered with filters that are equivalent to normal
surgical facemasks and/or N95 respirators
(Li et al 2004)
. It is
expected that such separation in facemask design would
reduce the contamination of inhaled air and increase the
protective efficiency of facemask to the wearers compared
with commercially available surgical facemasks. The
principal objective of this study was to examine the
hypothesis of how the virus-laden respiratory droplets transmit
through facemasks and the protective efficiency of two
types of new facemasks with separated breathing pathways
from the virus-contaminated areas. For comparison, we also
examined the filtration efficiency of commercially available
Ten healthy subjects were advised of all aspects of the
investigation, including the nature, purpose, method, and risks
of the study, and consented to participate in the study. The
subjects were five men and five women, aged 21–41years
(mean 28.7 ± 6.9 SD). Other physical characteristics (mean ±
SD) of the subjects were as follows: height, 170.4 ± 7.1 cm;
weight, 64.4 ± 8.4 kg; body surface area, 1.71 ± 0.14 m2.
The experimental protocol was approved by the Human
Subject Ethics Sub-committee of The Hong Kong Polytechnic
University, and all procedures involving human subjects
complied with the Declaration of Helsinki (2000).
Figure 3 illustrates the two types of facemasks used in this
(Li et al 2004)
. Facemask A was made of
laminated polypropylene with polyester fabrics with two exhaust
valves made of plastic and situated at its back. The exhalation
valves open to release exhaled air and close during inhalation.
The inhalation valves perform in the opposite way, opening
during inhalation and closing during exhalation. Fresh air
enters into the mask through two inhalation valves covered by
a filter that is made from the same fabric as a surgical facemask
to prevent microbes or other toxic substances from entering
the respiratory tract by inhalation. Facemask B was also made
of laminated polypropylene with polyester fabrics and had
two exhaust holes situated at its back. The wearers respired
through the same two exhaust holes covered by filter
materials, which was also made from the same fabric as a surgical
facemask. The major difference between Facemasks A and B
was that the former had exhaust valves, but the latter did not.
The surgical facemask was commercially available for use in
public hospitals and clinics in Hong Kong. The tested surgical
facemask was about 0.80 mm thick, and facemasks A and B
were about 2.45 and 2.41 mm thick, respectively.
Viral loading simulation
The study utilized the same experimental setup that used
in previous experiment
(Li et al 2006)
solution was used to simulate viral aerosols, as it would be
dangerous and unethical to conduct in vivo facemask tests
by exposing human participants to live viruses. Both KCl,
one of the main cations in body tissue, and Fluorescein, a
diagnostic adjunct used in retinal angiography, are not known
to be harmful to the human body and are injected into veins
in clinical practice (Ford 1996). The use of KCl rather than
NaCl as suggested by the NIOSH for the test challenge
is because the concentration of KCl
in human sweat is very low and has minimum effect on the
in vivo test results
(Zhang and Qiao 1997)
. The fluorescent
stain was mainly used to simulate extends of viral
contamination, instead of the live virus. In this study, simulated viral
particles were produced by the nebulization of a
Fluorescein-KCl solution with a concentration of 2 mg of KCl and
0.003 mg Fluorescien/cm3 of deionized water. An atomizer
was used to generate simulated viral aerosols by spraying
the Fluorescein-KCl solution. Assuming the density of the
solution is 1, the average weight of splash in one stroke of
spray was 1.27 g, as weighed with an electronic balance that
has precision of 0.001 g.
The subjects entered a climatic chamber, which was
maintained at 25 °C and 70% of relative humidity, which was
similar to the working environment of hospitals. Before
commencing exercises, the participants sat in a chair for 30
minutes, during which they were asked to drink 500 ml water,
then put on a randomly selected facemask.
In order to sample the amount of droplets on the
facemask, a piece of 22.5 mm filter paper was affixed at the outer
and inner surface of facemasks A and B, respectively.
The subjects then performed intermittent activities
including exercise (E1), rest (R1), exercise (E2), rest (R2),
exercise (E3), and rest (R3) on a treadmill at the walking
speed of 3.2, 4.8, and 6.4 km/hr, respectively. Except at E1
(20 min), activities lasted for 10 min. The workloads at a
level walking speed of 4 km/hr represented approximately
23% of maximum work capacity when the subjects did not
wear any protective equipment (calculated on the basis of
the initial maximal exercise tests)
(White et al 1991)
this period, the researcher sprayed a KCl-Fluorescein solution
as to stimulate a viral solution onto the facemasks twice at
a distance of 100 cm every 10 minutes. The simulated viral
solution was sprayed on the facemasks 14 times in total
during both walking and resting.
The participants took off the facemask at the end of the
experiment. Upon completion of the exercises, the outer and
inner surfaces of the facemasks were UV scanned and had the
fluorescent stains photographed, as shown in Figure 4. After
completing the facemask trial, the surgical facemask,
facemask B, and filter paper samples of the outer and inner surface
of facemasks A and B were collected. The surgical facemask
and facemask B were separated into three layers. Different
layers and filter paper samples were put into different beakers
and 50 ml of distilled water were added. The samples in the
water were stirred intermittently for 15 minutes. Then the
solutions were filtered with filter paper to eradicate the fine
fibers from the solution. The solutions were tested with the
Clinical Flame Photometer 410 C instrument (Corning Inc,
Corning, NY, USA).
Before testing the samples, calibration curves for KCl
were obtained experimentally. Solutions with the KCl
concentration of 0.02%, 0.01%, 0.005%, 0.0025%, 0.0012%, and
0.00062% were prepared and then were tested on the Clinical
Flame Photometer. Five readings of each known solution
were recorded from the instrument and the average was
calculated. With readings from the photometer and the known
K+ concentration, the data values were plotted and analyzed
to derive calibration curves and equations, which were then
used to determine the concentrations of test samples from the
photometer measurements. For every facemask, the data for
each layer also shows K+ content of the layer in percentage.
Further, the relative K+ content of each layer to K+ content of
the whole mask was calculated by dividing the K+ content of
each layer with the sum of K+ content of all layers for each
facemask. Percentages were used as the basis for analysis
of the test results for three layers of surgical facemask and
facemask B, and two layers of facemask A.
A study comparing the effects of wearing different kinds
of facemasks (N95, surgical, and facemasks A and B) on the
ear canal temperature, heart rate, and clothing microclimates
was carried out simultaneously
(Guo et al 2006, 2008)
addition, after wearing the facemask for 100 min, the subjects
were asked “how do you like the mask?” The scales ranged
from 0 to 10, with “0” representing “not at all”, “5”
representing “acceptable”, and “10” representing “very fond of”.
As the relative K+ content (%) of the inner layer of the
facemasks is a key parameter indicating protective effects
of facemasks, we used this parameter to estimate the sample
size. According to our preliminary experiment, the difference
between the two kinds of facemasks in the relative K+ content
(±SD) is about 1.25 (±0.7)%. Based on this data, the required
sample size was found to be 10 participants in order to have
a P value 5% and a power of 90%.
Univariate analysis of variance and one-way ANOVA
were conducted to determine whether the factors had
significant effect. Dependent variable is the relative K+
content, and factor is facemask/filter paper sample layers
and/or facemask types. P values
0.05 were considered
Figure 5A showed the comparisons of different facemasks
in the relative K+ content in outer and inner filter papers
of facemasks A and B. The front surface of facemask A
captured 98.9% to 99.9%, and the front surface of facemask
B captured 99.4% to 99.8% of the K+ solution. Only 0.1% to
1.1% and 0.2% to 0.6% of the K+ solution could penetrate
and reach the inner surfaces of facemasks A and B. By
carrying out the analyses of the variances on the K+ values,
we found that there are no significant differences in relative
K+ content between the two types of facemasks, but there
were significant differences in relative K+ content between
the layers. Relative K+ content was significantly lower in
inner filter papers than in outer filter papers for the two types
of facemasks (P 0.001). On the basis of K+ content in outer
and inner filter papers of facemasks A and B and in face skin
of subject, the relative K+ content of face skin of subjects is
0.06% to 0.6% wearing facemasks A and B.
Filter paper layer
Figure 5B compared the facemasks in the relative K+
content in outer and inner layers in surgical facemask and
facemask B. The outmost layer of facemask B had the
highest relative K+ contents (93.8% to 99.4%), which was much
higher than 80% to 82% relative K+ contents of the surgical
facemask. At the innermost layer of facemask B, there were
only 0.2% to 0.5% of the relative K+ contents, while the K+
relative contents of the innermost layer of surgical facemask
were 3.0%~4.5 %, showing that facemask B had significantly
higher protective efficiency (P 0.001).
On the basis of K+ content in each layer and the weight
of each stroke of spray, the actual amount of K+ was
calculated for each different layer. The actual amount of K+ (mg)
was 21.66 and 28.2 mg of K+ on average in the outmost
layer of the surgical facemasks and facemasks B; 0.79 and
0.135 mg of K+ were on the innermost layer of the surgical
facemasks and facemask B. For filter paper samples, the
actual amount of K+ (mg) was 9.79 and 10.64 mg of K+ on
average in the outmost layer of the facemasks A and B; and
0.027 and 0.033 mg of K+ were on the innermost layer of
the facemasks A and B.
As there were limited products, facemask A couldn’t be
cut and separated three layers to measure. Therefore, the
actual amount K+ of facemask A was estimated from filter
paper samples. But the results from facemask B proved that
the method sampled by using filter papers had similar test
results on filtration efficiency comparing with those obtained
by using three layers of facemask (Figure 5A).
Areas of contamination
Different areas of the facemasks in relative K+ content were
compared in Figure 6. Figure 6 showed much higher
relative K+ content in the filter papers on the front surface of the
facemasks in comparison with that in the surgical facemask
filters covering the exhaust valves/holes at the back of
the facemasks. 92.3% to 98.9% of droplets for facemask A
and 98.7% to 99.5% of droplets for facemask B were blocked
by the front surface of the facemasks, whereas only 1.1%
to 7.7% of droplets for facemask A and 0.5% to 1.3% of
droplets for facemask B reached the back of the facemasks.
Relative K+ content was significantly lower in the back of
the facemasks than in the front surface for the two facemasks
(P 0.001). Relative K+ content of the surgical facemask
filters covering the ventilation valves/holes at the back of
the facemasks were 0.6% to 5.8% and 0.3% to 0.7% (outer
layer), 0.3% to 1.5% and 0.1% to 0.4% (middle layer), 0.2%
to 0.4% and 0.1% to 0.2% (inner layer) for facemasks A
and B, respectively. The experimental results presented in
Figures 5 and 6 are summarized in Figure 7.
In addition, for the surgical facemask filters covering
the exhaust valves/holes at the back of the facemasks, the
relative K+ content was significantly lower in inner layer
Front (filter paper)
Back (middle filter)
Back (outer filter) Back (Inner filter)
The front surface and back of the masks and filter layers
filters than in outer layer filters for facemasks A and B
(P 0.001), showing that the exhaust valves/holes were
To test whether KCL concentration measured in
individual layers of masks using this KCl solution test method is
influenced by KCL concentration in human sweat, the sweat
from the face and back skin surface just after taking off each
testing mask were collected. KCL concentrations in the sweat
were measured in the same way. The results showed that the
KCL concentrations in the sweat from face and back skin
surfaces were much lower than that measured in the layers of
the masks, indicating that the KCl solution test method was
not affected by the KCL concentration in the sweat.
Fluorescent stains test
As Figure 4 shows, the entire front surfaces of facemask B
and most front areas of facemask A and the surgical
facemask were contaminated by simulated droplets. On the inner
surfaces of facemasks A and B seen in Figure 4, we could
not find any contamination of fluorescent stains. On the
other hand, some fluorescent stains were found on the inner
surfaces of the surgical facemask. These results indicated
that, in practical working conditions, virus-laden respiratory
droplets penetrated and contaminated the inner surfaces of
surgical facemask, but could not penetrate and contaminate
the inner surfaces of facemasks A and B. These visual
observations agreed with the quantitative measurements on
the K+ concentrations.
The acceptability of the newly designed facemasks
The rated mean values of the answers to “how do you like the
mask?” were 5.4 and 4.8 for facemasks A and B, respectively,
suggesting that facemask A can be accepted and facemask
B came in as a close second acceptance.
This study aims to obtain experimental evidences to illustrate
the aerobiological pathway of virus-contaminated aerosol
through facemasks to guide and improve the design of
facemask for enhancing protective efficiency of facemask. There
are a number of critical findings that may have significant
clinic implications in hospital infection control practices
when communicable respiratory infections are transmitted
by means of large droplets over short distances:
• Around 92.3% to 99.5% of droplets were blocked by the
front surface of the facemasks. This shows that the front
surface of the facemask receives most of the
contaminated droplets when HCWs speak to and/or take care of
patients (Figure 7). These observations provide direct
experimental data to support the guidelines recommended
by the WHO and Centers of Disease Control (CDC),
ie, to use a facemask to provide respiratory protection
against infectious respiratory diseases such as influenza,
tuberculosis, or SARS
(CDC 1993, 2005; WHO 2003)
• As more than 90% of the simulated viral loadings were
blocked by the front surfaces of the facemasks, the inhaled
air could be contaminated with viruses if the breathing
pathway overlaps the viral-contaminated areas, and then
the efficiency of the filters becomes the only protection
for the wearers.
• There are huge differences in the simulated viral
contaminations on the front and back surfaces of
facemasks. Only 0.5%~7.7% of droplets reached the
back of the facemasks. Therefore, it is critically important
to separate the breathing pathways from the
viruscontaminated front surface.
• By simply locating the breathing pathways to the back of
facemask and using the same filters of surgical facemask,
the in vivo protective efficiency of facemasks A and B
reached 98.9% to 99.9% compared with that of normal
surgical facemasks of 95.5% to 97.0% for KCl particles.
The differences of 2.9% to 3.4% in the protective
efficiency of facemasks may have important implications
for doctors and nurses who are exposed to critically ill
patients. With a fit test to ensure good fitting, it can be
expected that the protective efficiency of facemasks A
and B can be further increased.
These findings maybe applicable to the airborne
transmission in relative stable air streams, as the airborne particles
with size range of 0.1 to 100 µm are significantly heaver
than air, thus they would likely drop to the ground in time.
Their pathways would be expected to be similar with those
of droplets shown in Figure 1. Therefore, the chances for
the airborne particles to reach the back and/or bottom of a
facemask would be lower than those to reach the front surface
of the facemask. This means that separation of the
breathing pathways from the front surface could still effectively
increase the protective efficiency of facemask for airborne
transmissions. It is different story in the cases of turbulent
These experimental findings may have significant clinic
implications for infection control in hospitals and community
settings. Lee and colleagues (2003) reported the infection of
SARS to 85 HCWs and students after exposure to the index
patients. Svoboda and colleagues (2004) concluded that the
transmission of SARS in Toronto was limited primarily to
hospitals and households that had contact with patients.
Seto and colleagues (2003) and Loeb and colleagues (2004)
reported that wearing facemasks with appropriate level of
protection efficiency was the most significant measures to
reduce the risk of infection of SARS. These cases highlight
and confirm the belief that most communicable
respiratory infections are transmitted by means of large droplets
over short distances or through contact with contaminated
surfaces. Therefore, it is critically important to increase the
protective efficiency of facemasks to protect HCWs and/or
people in community healthcare settings, and households
who have to take care of index patients with close contact.
Particularly, face-to-face consultation and care are the
necessary operations in the treatment of patients with respiratory
transmitted diseases, who expel frequently contaminated
particles from the lower and upper respiratory tract by violent
expirations such as cough, sneeze, or simple exhalation.
Moreover, the ventilation properties of facemasks
A and B reduce in significantly different temperatures and
humidity in the microclimates of the masks and increase the
heat loss of the body, which is responsible for reduced heart
rate, blood pressure, and thermal stress compared with N95
(Guo et al 2006, 2008)
. Furthermore, facemasks
A and B can or almost can be accepted by wearers
et al 2008)
. These results implicate the favorable usability
of facemasks A and B.
Therefore, we conclude that when droplets spread onto
a person in a face-to-face position, the entire front surface
or most front areas of facemask were contaminated. More
than 90% of droplets are blocked by the front surface of
facemask. Only 0.5% to 7.7% of the droplets reach the
back of facemask. Separating the breathing pathways from
the virus-contaminated areas could contribute to the higher
protection efficiency of facemasks to 98.9% to 99.9% by
using normal surgical facemask filters.
This project was supported by research grants G-U027, A188,
and A174 of the Hong Kong Polytechnic University. The
authors report no conflicts of interest.
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