Eco-Environment & Health 1 (2022) 3–10

Contents lists available at ScienceDirect

Eco-Environment & Health

Review

SARS-CoV-2 aerosol transmission and detection

A R T I C L E I N F O A B S T R A C T

Keywords: Aerosol transmission has been officially recognized by the world health authority resulting from its overwhelming
Aerosol transmission experimental and epidemiological evidences. Despite substantial progress, few additional actions were taken to
SARS-CoV-2 prevent aerosol transmission, and many key scientific questions still await urgent investigations. The grand
Exhaled breath
challenge, the effective control of aerosol transmission of COVID-19, remains unsolved. A better understanding of
Aerosol detection
the viral shedding into the air has been developed, but its temporal pattern is largely unknown. Sampling tools, as
one of the critical elements for studying SARS-CoV-2 aerosol, are not readily available around the world. Many of
them are less capable of preserving the viability of SARS-CoV-2, thus offering no clues about viral aerosol
infectivity. As evidenced, the viability of SARS-CoV-2 is also directly impacted by temperature, humidity, sun-
light, and air pollutants. For SARS-CoV-2 aerosol detection, liquid samplers, together with real-time polymerase
chain reaction (RT-PCR), are currently used in certain enclosed or semi-enclosed environments. Sensitive and
rapid COVID-19 screening technologies are in great need. Among others, the breath-borne-based method emerges
with global attention due to its advantages in sample collection and early disease detection. To collectively
confront these challenges, scientists from different fields around the world need to fight together for the welfare of
mankind. This review summarized the current understanding of the aerosol transmission of SARS-CoV-2 and
identified the key knowledge gaps with a to-do list. This review also serves as a call for efforts to develop
technologies to better protect the people in a forthcoming reopening world.

1. Introduction ago. As of April 20, 2022, more than 504 million COVID-19 infections
including 6.2 million deaths, were reported [14]. As of April 17, 2022, a
In human history, there has been an evolving understanding of the large fraction of people in the world had already been vaccinated with a
airborne transmission of infectious diseases [1–6]. Back in the AD total of 11.3 billion doses of vaccine administered globally [14]. Unfor-
100–200, a miasma theory proposed by Roman physician Aelius Galenus tunately, studies have shown that vaccinated people could still get
described the airborne transmission of infectious diseases. Then about infected by variants of SARS-CoV-2 [15,16]. In the coming months,
500 years ago, Italian physician Girolamo Fracastoro (1478–1553) stated people are still afraid of society reopening after the pandemic hit [17,18].
in his book that airborne tiny particles can cause epidemic diseases over a How to effectively prevent infection of COVID-19 is a rather important
distance. Later, Louis Pasteur (1861) discovered viable microorganisms question in the face of a complete reopening global economy.
in the air that could propagate under nutrient conditions [7]. It is now Aerosol transmission plays a major role in many large-scale infectious
known that the air we breathe consists of microbes, either viable or dead, disease outbreaks, including COVID-19 [10]. Developing a better un-
together with their derivatives such as endotoxin and allergens [8,9]. derstanding of the role of aerosol transmission of SARS-CoV-2 can help
With every breath, we inhale various microorganisms from the air. When counter the threat. On the other hand, SARS-CoV-2 aerosol detection can
a pandemic occurs, airborne transmission of certain respiratory viruses serve as a “smoke detector” for COVID-19 such that early-stage control
could quickly dominate the spread [4,10]. In addition, climate change measures can be implemented before the disease starts spreading further
further deteriorates air pollution, and the frequency of infectious out- in the community. Additionally, rapid screening of people for COVID-19
breaks also increases [11,12]. It has been long anticipated that there will can help locate the infected in time. Currently, effective control often
be a global infectious disease outbreak in the distant future [13]. Such a requires lengthy quarantine, which is difficult to implement for the
moment, the COVID-19 pandemic, finally struck the world three years reopening economy. People would face greater risks of COVID-19

yao@pku.edu.cn.

https://doi.org/10.1016/j.eehl.2022.03.001
Received 27 November 2021; Received in revised form 2 March 2022; Accepted 13 March 2022
Available online 15 April 2022
2772-9850/© 2022 The Author(s). Published by Elsevier B.V. on behalf of Nanjing Institute of Environmental Sciences, Ministry of Ecology and Environment (MEE) &
Nanjing University. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
M. Yao Eco-Environment & Health 1 (2022) 3–10

infections in the opening economy. On-site SARS-CoV-2 monitoring and transmission. It is time to re-consider this important indoor health
rapid COVID-19 screening are two key technological shields for pro- problem. If the aerosol transmission can be better controlled, the impact
tecting people from infection in combating the pandemic. However, of the pandemic could be substantially minimized.
these two critical components are under-studied and need to be rapidly
developed in the face of massive challenges for reopening the economy. 3. Microbial aerosol sampling
Time for these efforts is rather limited, and key actions must be taken
immediately. However, all these developments require a deep under- 3.1. Bioaerosol sampling
standing of the key issues relevant to aerosol transmission. Here, a review
was conducted to summarize current advances in understanding the SARS-CoV-2 aerosol monitoring is critical to guarding the air. Among
problems and technological solutions and to identify the key knowledge others, sampling is the first step for characterizing the risk. Over the
gaps with a to-do list for combating the COVID-19 pandemic. years, many efforts have been devoted to air sampling for viruses, bac-
teria, fungi, and other biological aerosol materials [40]. There are many
2. SARS-CoV-2 emission and aerosol transmission different types of samplers for collecting bioaerosol particles. Each one
has its own advantages and disadvantages [41]. Virus sampling usually
COVID-19 patients were found to emit millions of SARS-CoV-2 par- requires a very low cutoff size (the particle size at which the sampler has
ticles per hour, especially during the early stage of the disease [19]. a 50% collection efficiency) because the viral particles are usually much
SARS-CoV-2 concentration levels in the exhaled breath condensate were smaller than bacteria and fungi. When the viral particles are released into
also shown to vary among individuals [19]. SARS-CoV-2 can be released the air from human breath, they evaporate and are diluted quickly by the
via exhalation, talking, coughing, sneezing, or other means into the atmosphere. Accordingly, a large air volume has to be collected to enrich
environment, for example, directly into the air, onto surfaces, or into enough viral nucleic materials for PCR amplification. Additionally, since
wastewater [20–23]. Those deposited on surfaces could be re-aerosolized the air is moving even in indoor environments and so do particles, the air
into the air upon evaporation and walking disturbance [24–26], while sampling has to be very rapid so that enough air volume can be obtained
those in the water could also be re-aerosolized into the air, for example, in a very short period. Despite the high physical collection efficiency of
during the toilet flushing process [27]. Leung [28] provided a thorough filtration, collecting a large air volume is a great challenge due to its low
review of different transmission modes. In the aerosol science field, we sampling flow rate and high pressure drop. In addition, the strong
refer to aerosol as a mixture of particles of less than 100 μm in a gaseous physical desiccation from the filter is another problem, especially for
medium [29]. Here, we use the term from the aerosol science community viral infection studies. A liquid sampler can somehow satisfy both high
to describe disease transmission, referring to not just those of less than volume and viability preservation requirements.
5 μm, but also larger ones (<100 μm). Accordingly, the air is a vital
exposure route to SARS-CoV-2 for humans. 3.2. SARS-CoV-2 aerosol sampling
As of this writing, the SARS-CoV-2 emission patterns remain unclear.
He et al. [30] reported that the highest viral load in throat swabs was During the early stages of the COVID-19 pandemic, our research team
observed at the time of symptom onset, and transmission of COVID-19 has employed a robot-assisted cyclone sampler for automatic sampling of
occurred at the presymptomatic stage. Ma et al. [19] also showed that airborne SARS-CoV-2 in hospital environments [22]. We have success-
COVID-19 patients in the early stages emitted more viral particles than fully collected SARS-CoV-2 with a concentration level of 9–219 RNA
the late ones. Some studies showed that the infectiousness increased copies/m3 [22]. The air sampler collected 18 m3 of air from 40-min
about 1–5 days after symptom onset of COVID-19 [31], which varied sampling. In another independent work, the cyclone sampler also suc-
greatly among individuals [31,32]. In our previous work, even right cessfully collected SARS-CoV-2 with a level of 1.11  103 to 1.12  104
before the hospital discharge, the COVID-19 patients’ exhaled breath still RNA copies/m3 [42]. Other teams have used filters, e.g., gelatin filters,
contained SARS-CoV-2 RNA [22]. Our previous studies have shown that which needed a longer sampling time (e.g., up to 20 h) to obtain enough
human breathing produces particle emissions of 1.5 μm peak size [33]. volume of air [25], and a ventilation duct to collect the virus [19,22,43,
Fennelly [34] reviewed available studies and found that cough aerosols 44]. In another work, sampling with a high flow rate (50 L/min) filter
and those of exhaled breath from patients with various respiratory in- was also used for detecting SARS-CoV-2 [45]. These methods have their
fections had similar aerosol size distributions, that is, a predominance of own advantages and depending on the actual situation the desired
pathogens in small particles (<5 μm). However, the expelled particle size sampling method can be selected. The use of a ventilation duct is similar
distribution of aerosols from COVID-19 patients is still not available at to an air sampler, but it is difficult to quantify the viral level in the air.
the time of this writing. Zhao et al. [35] found that speech-generated However, in order to obtain a result in a very short time, a large volume
droplets can spread three times farther in low-temperature and of air by rapid sampling is certainly preferred. When designing a sampler,
high-humidity environments, and in contrast, the number of aerosol ideally both physical and biological collection efficiency should be
particles increases in high-temperature and low-humidity environments. considered. As discussed above, a critical parameter for characterizing a
SARS-CoV-2 emissions depend on many different factors, for example, sampler’s physical efficiency is its cutoff size. Biological collection effi-
disease stage, time of the day, medication use, age, etc. [19,36,37]. ciency, on the other hand, refers to its ability to collect viable biological
Accordingly, SARS-CoV-2 emission uncertainty impacts the polymerase aerosol particles.
chain reaction (PCR) test. Similar to wastewater-borne viral monitoring [46], SARS-CoV-2
Airborne SARS-CoV-2 emission plays a very important role in the aerosol sampling in a public space can be used as a pooled sample of
COVID-19 transmission. After a long, heated debate, the WHO finally exhaled breath from many different people who spent time in the envi-
stated that the airborne route is an important transmission route for ronment. Therefore, one air sample can serve as a surrogate sample for
COVID-19. In contrast, studies have indicated the fomite-facilitated many people in an enclosed or semi-enclosed space. SARS-CoV-2 pres-
transmission plays a minor role in the COVID-19 pandemic [38,39]. ence in the air sample means that there might be a COVID-19 patient who
Central to the debate is the difference in the definition of aerosol and spent time in the studied environment. For example, a liquid sampler
droplet [1]. It is now widely accepted that aerosol transmission plays a (Beijing BioCTech Co. Ltd) was employed to monitor SARS-CoV-2 aerosol
very important role in this pandemic. There is a collective call for con- in Beijing Winter Olympic Games. SARS-CoV-2 in the air is usually
trolling indoor respiratory infections through both ventilation and en- diluted and dispersed over time, thus a method with a lower detection
gineering control methods [2]. In the future, building design should take limit is desired in order to detect a minute number of viral particles. Air
into account aerosol transmission, for example, ventilation, solar inacti- sampling and detection together can serve as a warning for air safety so
vation of pathogens, and a toilet system that minimizes aerosol that disinfection and control measures can be mounted immediately

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before any further spreads. Future sampling protocol needs to be air sampling, microfluidics, silicon nanowire sensing, and electronics for
designed so that the infectivity of viral particles can be better preserved real-time monitoring of airborne influenza virus. The system translates
for subsequent infectivity analysis. In addition to environmental moni- airborne biohazard into a viewable electrical signal which renders
toring, wearable sampling devices can also be developed for personal humans equivalently equipped with additional “sensing capability” for
breathing zone monitoring to assess the personal exposure risk. In the the airborne biohazard. Many similar nano-enabled technologies can be
pandemic era, SARS-CoV-2 aerosol monitoring becomes particularly utilized for SARS-CoV-2 detection when coupled with air sampling for
important and can be used for the early detection of a potential aerosol [52]. Similarly, this can also be achieved for real-time monitoring
COVID-19 outbreak. of SARS-CoV-2, as illustrated in Fig. 1. The air is continuously sampled,
and transported by a peristaltic pump via microfluidics into the
4. SARS-CoV-2 aerosol detection strategy antibody-decorated sensor area. Whenever there is SARS-CoV-2 in the
air, the sensor would generate a viewable electrical signal that can serve
4.1. Nucleic acid-based SARS-CoV-2 aerosol detection as an alert. Such technologies may have great potential in combating
airborne infectious disease threats, for example, this COVID-19
There is a heated debate about the aerosol transmission of COVID-19. pandemic. Yet, there is still a long way from the laboratory to practical
This debate is largely due to the differences in disciplines and the lack of sensing. With challenges from COVID-19, this area of research now
aerosol detection methods. Unlike pollutants in other media, airborne would certainly need to move faster than any other time.
pollutant detection has to come with well-performed air sampling first. Ideally, a wearable sensor device can be developed to alert potential
For SARS-CoV-2 aerosol detection, the common practice is to combine air exposure risks. Relevant technologies are already there, and what needs
sampling with a nucleic PCR test. With respect to sampling, a momentum to be done is to integrate various elements and optimize the performance.
was observed that a cyclone liquid sampler with a high flow rate is For example, a wearable device was developed for sensing SARS-CoV-2
generally preferred to collect SARS-CoV-2 aerosol, especially in China. As by integrating several elements such as substrates and textiles function-
for RT-PCR tests, they have been reported to fail to detect SARS-CoV-2 in alized with freeze-dried, cell-free synthetic circuits, and CRISPR-based
many air samples due to their high detection limits [19,22,25]. Occa- tools [53]. At the same time, antibody-based sensing needs robust virus
sionally, air samples collected from toilets (a confined and enclosed receptor and background noise reduction algorithms. Additionally, better
environment) were tested positive by RT-PCR with a higher viral RNA sensing sample pretreatment technology might also be required after the
level [19,45]. On the other hand, Loop-mediated isothermal amplifica- sampling to enhance the detection capability. On-site stable and reliable
tion (LAMP) has a relatively lower detection limit and a higher sensi- detection of SARS-CoV-2 aerosol in real-time could play a critical role in
tivity, and has been increasingly used for detecting SARS-CoV-2 [47]. guarding against the pandemic. Unfortunately, such a system is still in its
Indeed, it can be used together with air sampling for SARS-CoV-2 aerosol bench stage as of this writing.
detection, which can provide an early warning for a potential COVID-19 Air is a complex mixture of thousands of different biological and non-
outbreak. biological pollutants, and many of them are not identified due to the lack
of analytical power. The guard against air toxicity is a significant chal-
4.2. Other sensors and detection methods for SARS-CoV-2 lenge not only for now but also in the future. Toward this end, a recent
work has demonstrated some promise of real-time monitoring of air
Concurrently, other studies investigated the use of immune-based, toxicity by utilizing volatile organic compounds (VOC) profile emitted by
nanosensor, and optical methods for rapid SARS-CoV-2 detection a mouse when exposed to different toxic substances [32]. They have
[48–50]. These technologies, although ultra-sensitive and fast, have not shown that whenever the mouse was exposed to a toxic airborne sub-
been utilized in the real-time monitoring of SARS-CoV-2 aerosol. Prac- stance, it would release a distinctive profile of VOC fingerprints within a
tically, online detection of SARS-CoV-2 can be very useful in guarding air very short period. If further improved and optimized, the system could
safety in public domains. Airborne detection of pathogens has been a monitor those unknown human pathogens. This type of sensing repre-
long-standing challenge for many years. Shen et al. [51] have integrated sents a future need for comprehensive air toxicity monitoring.

Fig. 1. Integration of commercialized technologies, including air sampling, microfluidics, and antibody-decorated silicon nanowire sensor for real-time monitoring of
SARS-CoV-2 aerosol (photo provided by the author).

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5. SARS-CoV-2 aerosol viability and infection impacts of airborne pollutants on SARS-CoV-2, while environmental
scientists do not have the facility such as BSL-2 or that with a higher
5.1. Impacts of environmental parameters on SARS-CoV-2 infection safety level and resources to conduct relevant experiments. Certainly,
more efforts should be devoted to investigating the influencing factors on
Infection by SARS-CoV-2 depends on the dose and viability of SARS- the viability of SARS-CoV-2 in the air, which is critical to establishing an
CoV-2. For potential SARS-CoV-2 aerosol exposure, the concentration infection. The discovery of such factors can guide engineering design
decreases over a longer distance from the source. The overall dilution solutions for the indoor environment. This could help make a huge dif-
depends on the dimension of the indoor environments and the ventilation ference in defeating the pandemic, especially in a reopening economy.
characteristics. Increasing ventilation and distance would substantially Nonetheless, the study of the viability of airborne SARS-CoV-2 requires a
decrease the viral aerosol level, thus reducing the potential dose. SARS- better sampling method.
CoV-2 viability is equally important for establishing an infection. The
SARS-CoV-2 was shown to remain viable for a sustained period of up to 6. Experimental and epidemiological investigation of aerosol
16 h in respiratory size particles [54]. In other studies, viable transmission of SARS-CoV-2
SARS-CoV-2 was also recovered from hospital environments [55], pas-
senger cars [56], and respiratory mask surfaces [42]. When the virus is Since the pandemic, many teams have carried out epidemiological
released into the air, its surface spike protein would be in contact with air investigations for outbreaks. Environmental transmission plays an
pollutants (particles and gaseous pollutants such as ozone, NOx, etc.). important role [68], especially the airborne route. Recently, in Guangz-
Likewise, the virus would be also surrounded by ambient pollutants hou COVID-19 outbreak, there was a simulation report that the
when deposited together inside the lung. During the initial phase of the COVID-19 was transmitted between two “handshake” buildings (i.e.,
pandemic, Yao et al. [57] analyzed the effects of environmental param- buildings that are very close to each other) via an airborne route [69]. An
eters such as ozone, humidity, and temperature on the COVID-19 spread. overseas traveler stayed in an observation room waiting for his RT-PCR
It was shown that the number of COVID-19 cases increased with test results, while simultaneously transmitting the SARS-CoV-2 into the
decreasing ozone levels (94.67–48.83 μg/m3). By contrast, the number of room of another close building (about 0.5 m distance) across the space
cases increased with increasing relative humidity (23.33%–82.6%) but between the two buildings. A lady in the other building got infected via
decreased with increasing temperature [57]. Ozone was verified to inhalation of the transmitted viruses. A gas tracer study led by our group
inactivate SARS-CoV-2 effectively [58,59]. Other studies showed that on May 29, 2021, has found that the exhaled virus can be easily trans-
ultraviolet-C (UV-C) can efficiently inactivate SARS-CoV-2 [60,61]. mitted into the other building, as demonstrated in Fig. 2. About 5%–18%
These environmental parameters together play a role in the viability of of the tracer gas released at location A entered the clinic room in Building
SARS-CoV-2 aerosol. Thus, cities with different matrices of these pa- #2. According to the epidemiological report, the lady who got infected
rameters could have different COVID-19 transmission potentials. Because did not have any previous close contact with the COVID-19 patient. This
of damages from air sampling, culturing SARS-CoV-2 is difficult. outbreak presents strong evidence for aerosol transmission of COVID-19.
Breathing by people is also a process of “air sampling” by which airborne In a bus COVID-19 outbreak, the airborne spread of SARS-CoV-2 was
particles deposit into the lung, but it is gentler compared with air sam- likely to contribute to the high attack rate [70]. The central air condi-
pling with minor damages to the virus viability. Nonetheless, sharing tioners for both buses were in indoor recirculation mode. Many more
both space and time with COVID-19 patients would significantly increase similar outbreaks point to the airborne transmission of COVID-19 [71,
the infection risk. This, on the other hand, could explain the discrep- 72]. Epidemiological evidence for airborne transmission sometimes re-
ancies among the effects of environmental parameters, air sampling, and quires solid proof from the nucleotide sequence of SARS-CoV-2 in sam-
inhalation on the SARS-CoV-2 viability and infection. ples from different COVID-19 patients. For example, a study has linked
the COVID-19 outbreak to environmental transmission via cold-chain
5.2. SARS-CoV-2 aerosol viability food supply, which did not exclude the possible aerosol transmission in
Xinfadi Market in Beijing based on sequencing data [73]. However, the
The viability and culturability of SARS-CoV-2 are largely related to its air is moving, and in-situ direct evidence cannot be obtained for humans
receptor-binding domain (RBD) residing on the spike protein, which for ethical reasons.
binds to the human angiotensin-converting enzyme 2 (ACE2) receptor Since the pandemic, many studies have presented evidence of
[62]. Anything that can influence the binding of the RBD with ACE2 airborne transmission of COVID-19 using animal models [74,75]. For
impacts the cell entry ability of SARS-CoV-2 and its infection. As example, Kutter et al. [76] have shown that both SARS-CoV and SAR-
mentioned above, SARS-CoV-2 in the air could interact with atmospheric S-CoV-2 can be transmitted through the air between ferrets over more
pollutants. Among them, some species such as ozone could directly than one-meter distance. It is a challenge when epidemiological inves-
degrade viral coat proteins and disrupt the viral structures, thus rending tigation for environmental transmission is conducted to trace the trans-
the viability loss [63]; while some other species could alter the receptor mission routes where both surface-borne and airborne could be
characteristics of the viral surface [64]. These interactions would lead to simultaneously involved. For example, Li et al. [77] provided both
the inability of SARS-CoV-2 binding to ACE2, thus limiting the infection. epidemiological and genome evidence about the environmental trans-
Watzky et al. [65] have reported that 50 chemicals in the air modulate mission of COVID-19 but could not differentiate between airborne and
the expression of ACE2 or human proteases that are important for surface-borne transmission. Another difficulty is the culturing of
SARS-CoV-2 cell entry. They have further demonstrated that environ- SARS-CoV-2 in environmental samples (air and surface swabs).
mental exposures could influence the expression of genes involved in Currently, there is still limited information and understanding about how
viral cell entry. Of course, atmospheric pollutants might also impact long SARS-CoV-2 residing on the surface or in the air remains viable in
other properties of SARS-CoV-2, such as the replication potential through real-world scenarios, and when the loss of viability occurs, for example,
damaging the viral RNA by atmospheric radicals. Woodby et al. [64] in the media itself or during the sampling process. Additionally, factors
provided a detailed analysis of the influences of air pollutants on the involved in recovering viable SARS-CoV-2 from the air samples are
pathogenesis and replication of SARS-CoV-2. An association of an in- largely unknown. These factors altogether complicate the environmental
crease in PM2.5 level with a higher infection rate of COVID-19 was also (via air or surface) transmission investigation. The exact inhalation dose
detected [66,67]. However, no experiments were conducted to investi- of airborne SARS-CoV-2 required for establishing an infection is not
gate the impacts of PM2.5 on the viability of SARS-CoV-2. known either. These critical questions hamper a better understanding of
Apparently, there is a lack of active collaboration between virologists the airborne transmission of COVID-19. These questions are also central
and environmental scientists. Virologists are generally not aware of the to the debate on aerosol transmission, which however receives

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Fig. 2. Layout of the buildings where the delta COVID-19 outbreak occurred in Guangzhou in May 2021 and the tracer gas investigation illustration. The letters A, B,
C, D, E, and F represent different locations in two buildings. Alcohol was used as a tracer gas and a flame ionization detector (FID) sensor was the detecting instrument.

inadequate attention with much fewer actions. To better confront the represents a different sample coming from the lower part of the lung,
evolving pandemic, efforts and resources need to be re-allocated to study which could provide additional information about infections. Of course,
aerosol transmission and to investigate engineering solutions to defeat different breath sampling protocol might collect different size range
the pandemic. These efforts are not only useful for a current pandemic particles, which could impact the results. Besides, LAMP, as mentioned in
but could also be invaluable in humans’ fight against future insults. previous sections, has lower detection limits for SARS-CoV-2 [47], and a
combination of these two methods would offer a promising alternative
7. COVID-19 screening strategy for mass screening of COVID-19 with higher sensitivity.

7.1. RT-PCR protocol 7.2. Breath-borne VOC protocol

People get infected when inhaling short- or long-range SARS-CoV-2 Recently, breath-borne VOC has been utilized to screen subjects for
aerosol. As of this writing, the primary strategy for mass screening of COVID-19 indirectly [79–82]. Chen et al. [32] first reported breath-borne
COVID-19 is to utilize RT-PCR together with pooled throat swab samples VOC biomarkers for COVID-19. Many studies have demonstrated the
(e.g., in China, usually 10 samples are mixed for one test). There are some promise of using breath-borne VOC for rapid screening of COVID-19 [81,
limitations of this strategy. There is a long waiting line for the sample 83,84]. Chen et al. [79] found elevated acetic acid and propanol levels for
collection, with a possibility of transmitting the disease to nearby people COVID-19, while acetone levels decreased compared to the healthy
in the line. The advantage of using throat swabs is that the samples from a control. On the other hand, increased acetone level was observed for
group of people can be pooled together for group analysis similar to non-COVID-19 respiratory infections. Chen et al. [32] have found that
airport security screening. The collection of the swab sample is fast, but twelve key VOC species can be used as a fingerprint of COVID-19
can cause some discomfort to people. For analysis of SARS-CoV-2, RT- compared to healthy people and other upper respiratory infections. In
PCR as a gold standard is generally employed worldwide. However, the addition, other methods have also been developed to screen COVID-19
major problem is that sometimes COVID-19 patients can have false- using exhaled breath such as proton-transfer-reaction mass spectrom-
negative PCR test results, thus presenting a significant infection control etry (PTR-MS), gas chromatography-mass spectrometry (GC-MS), and
challenge. Accordingly, a new and rapid method must be developed to nanosensor [81–83], as well as the use of sniff dogs [85]. For example,
supplement the current RT-PCR test to avoid false negatives. Exhaled Shan et al. (2020) used non-VOC-species-specific sensor arrays to screen
breath condensate was previously used to screen influenza infection by COVID-19. They were able to differentiate between COVID-19 and
integrating silicon nanowire sensors [51]. As discussed above, COVID-19 healthy subjects by coupling machine learning and their eight VOC sig-
patients were shown to exhale millions of SARS-CoV-2 particles per hour nals. Using PTR-MS, COVID-19 acute respiratory distress syndrome
in the early disease stage [19]. The use of exhaled breath condensate (ARDS) and non-COVID-19 ARDS patients were also successfully differ-
together with RT-PCR tests could offer an alternative for COVID-19 entiated by breath VOC profiles (four VOC species) [81]. It should be
screening. The advantage is that people do not have to wait for the stressed that breath-borne VOC diagnostics is also valuable for other
throat swabs to be taken by the personnel. The subjects themselves can respiratory infections and diseases even after the pandemic [32].
take an exhaled breath sample collection through devices made widely Humans have many receptors for environmental contaminants, and for
available, and simultaneously the procedure can reduce the risks of most of the time, unfortunately, the sensing goes unnoticed. For example,
cross-infection by cutting short the waiting line. In addition, exhaled humans have an endotoxin receptor—toll-like receptor 4 (TRL4), and the
breath condensate collection is generally more comfortable than taking bindings trigger many biological events until the signals have been
throat or nose swabs [78]. Meanwhile, exhaled breath condensate translated into inflammation biomarkers such as interleukin-6 (IL-6),

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tumor-necrosis factor-α (TNF-α), etc. [86]. During this process, distinc- COVID-19 and identify the knowledge gaps with a to-do list in protecting
tive VOCs could be released whenever the exposure occurs. Our recent against the aerosol transmission of COVID-19 in a forthcoming reopening
work has demonstrated that when rats were exposed to airborne pol- world. This review also calls for particular attention to aerosol trans-
lutants, including endotoxin, distinctive profiles of VOCs were found for mission control of COVID-19 and for a request to allocate relevant re-
different pollutants within a very short period [87]. In terms of COVID-19 sources to fill the knowledge and technology voids to better protect the
screening by VOCs, the developed method could be impacted by back- world from the ongoing pandemic.
ground levels, medication, underlying health problems as well as
possible vaccination. Together with machine learning algorithms, the Conflicts of interest
patterns of VOC profiles can be well studied so that minute changes can
be detected by the method. Exhaled breath samples can be treated the The author has declared no conflicts of interest.
same as blood and urine samples, as they contain a vast amount of disease
information. Future technologies should be developed to analyze bio-
markers from exhaled breath so that early signs of diseases can be Acknowledgments
detected.
This research was supported by the National Natural Science Foun-
dation of China (NSFC) Distinguished Young Scholars Fund Awarded to
7.3. Future point-of-care protocol
M. Yao (21725701) and NSFC grants (22040101, 92043302), and by a
grant (EKPG21-02) from Guangzhou Laboratory. Xinyue Li and Ying Tian
Future hand-held and affordable e-nose with high accuracy for sensing
contributed to the COVID-19 outbreak investigation in Guangzhou.
breath-borne biomarkers should be developed to screen a large number of
subjects for various diseases, including respiratory infections. Since the
pandemic, breath-based diagnostics methods have already attracted un- References
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