Journal of Cleaner Production 348 (2022) 131094

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Journal of Cleaner Production

journal homepage: www.elsevier.com/locate/jclepro

Antibiotic resistance genes in bioaerosols: Emerging, non-ignorable and

pernicious pollutants
Ping Chen a, b, Xiaoyan Guo a, b, Fengxiang Li a, b, *
a
Key Laboratory of Environmental Remediation and Pollution Control, College of Environmental Science and Engineering, Nankai University, Tianjin, 300350, China
b
Key Laboratory of Pollution Processes and Environmental Criteria, Ministry of Education, Tianjin, 300350, China

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

Handling Editor: M.T. Moreira Harmful effects of antibiotic resistance genes (ARGs) in water and soil have been widely studied. However, the
transmission and hazards of airborne ARGs has attracted insufficient attention. ARGs in the air are usually
Keywords: carried by bioaerosols, affected by weather conditions, and threaten human health through inhalation or intake.
Bioaerosol This review contributes to the literature on controlling ARG pollution in the air by focusing on the transmission
Antibiotic resistance gene
pathway, comprehensively analyzing factors influencing the generation and propagation of ARGs in bioaerosols,
Air pollution
and overviewing the sources of ARGs in bioaerosols. Additionally, the composite contamination of ARGs in
Composite contamination
Heavy metal bioaerosols including heavy metals and polyaromatic hydrocarbons is also proposed, which has been ignored in
Polyaromatic hydrocarbon previous studies and can complicate ARG control. Finally, the challenges and outlooks are addressed, which is
constructive for the development of technologies for antibiotic and airborne ARG contamination remediation and
blocking risk migration.

1. Introduction
Antibiotic resistance genes (ARGs) pose an emerging, uncertain
threat to public health and ecological risks, which have attracted
worldwide attention. They have been detected in water bodies, such as
surface water and groundwater (Sidhu et al., 2020); organic wastes such
as activated sludge (He et al., 2019), livestock manure (Qian et al.,
2018), and food waste (Liang et al., 2020b); and in the air (Zhang et al.,
2019). The extensive use of antibiotics is one of the main causes of ARG
pollution. These antibiotics produce selective pressureand lead to the
emergence of antibiotic-resistant bacteria (ARB) and ARGs (Yan et al.,
2019). According to Van Boeckel et al. (2015), the global consumption
of antimicrobials is estimated to increase from 63,151 to 105,596 tons
(67%) between 2010 and 2030, which will continue to increase the risk
of ARGs to human health and ecology. Even without anthropogenic
activity or antibiotics, the natural environment contains multiple func­
tional ARGs (Biswas et al., 2021). For example, wild animals, permafrost
samples (30,000–5000 years old), and individuals in isolated pop­
ulations not exposed to antibiotics have been found to carry ARGs
(Hernando-Amado et al., 2019). Therefore, even though the use of
antibiotics has been limited, the ARG pollution still exists and should be
concerned.
Although ARG contamination has attracted extensive attention, most
studies focus on the ARGs in water or soil and ignore the ARGs in bio­
aerosols. Bioaerosols are suspended particles derived from organisms,
which can be obtained from human activities such as wastewater
treatment plants (WWTPs) and natural environments such as volcanic
eruptions (Ruiz-Gil et al., 2020). According to Gandolfi et al. (2013), the
air contained 103 to 107 cells m− 3 microbial biomass, including fungi
and bacteria, which can cause diseases such as hypersensitivity pneu­
monitis and asthma (Selman et al. 2010) through inhalation, ingestion,
or skin contact and make humans acquire antibiotic resistance (Benami
et al., 2016b). Zhang et al. (2019) detected 29 ARGs, which varied with
time and mainly included blaTEM, sul3, and tetW in highly polluted air in
Beijing. Liang et al. (2020a) also found ARGs, such as tetA, amino­
glycoside resistance genes and mobile genetic elements (MGEs), in the
Pearl River Estuary, indicating the risk of ARG exposure to the human
body. Wastewater treatment plants (Yang et al., 2020) and livestock
farms (Ferguson et al., 2021) can also release many bioaerosols carrying
ARGs and endanger human health after entering the human body

Abbreviations: ARB, Antibiotic-resistant bacteria; ARGs, Antibiotic resistance genes; COVID-19, Coronavirus disease 2019; EPS, Extracellular polymeric substance;
HGT, Horizontal gene transfer; MGEs, Mobile genetic elements; MRGs, Metal resistance genes; MSW, Municipal solid waste; PAHs, Polyaromatic hydrocarbons;
WWTPs, Waste water treatment plants.
* Corresponding author. author.College of Environmental Science and Engineering, Nankai University 38 Tongyan Road, Tianjin, 300350, China. .
E-mail address: lifx@nankai.edu.cn (F. Li).

https://doi.org/10.1016/j.jclepro.2022.131094
Received 14 November 2021; Received in revised form 10 February 2022; Accepted 21 February 2022
Available online 3 March 2022
0959-6526/© 2022 Elsevier Ltd. All rights reserved.
P. Chen et al.
through transmission. Therefore, studying the generation and propa­
gation of ARGs in bioaerosols is necessary to mitigate airborne ARG
pollution and protect human health.
Compared with ARGs in water or soil, airborne ARGs have wider
transmission range, a wider sources and are affected by more factors,
which are more likely to pose a threat to human health. In recent years,
the studies on ARGs in bioaerosols shows an upward trend (Fig. 1).
Although a few of the articles have reviewed ARGs in the air, they did
not focus on the transmission (Gao et al., 2015b) and the compound
pollution of airborne ARGs (Gwenzi et al., 2022), which can expand the
spread of airborne ARGs and make pollution control more severe and
complex. In this review, the transmission, hazards, and compound
pollution of airborne ARGs are discussed in detail, which are essential in
reducing the ARG pollution in the air and reducing the harm to human
body. The sources of ARGs in bioaerosols are also summarized and the
factors affecting ARGs’ transmission in the air are analyzed, which
should be considered when taking measures to control ARG contami­
nation in the atmosphere.
2. Sources of ARGs in bioaerosols
ARGs in aerosols are extensive, including human activity such as
wastewater treatment plants, graywater, municipal solid waste landfill,
livestock farm, and medical industry and natural phenomena such as
volcanic eruptions. Fig. 2 shows the ARGs abundance and species in
quantity in bioaerosols that have been found in the environment
through selecting a representative example from each source. Further­
more, Table 1 lists ARGs and bacteria, potential carriers of ARGs in the
air from many different sources.
2.1. Wastewater treatment plants and graywater
Wastewater treatment plants are main hotspots of ARB and ARGs.
Many articles have reported ARGs, such as tetracyclines resistance
genes, which can reach 1011.17 copies/mL in wastewater from WWTPs
(Li et al., 2016). By collecting aerosols produced by various processes in
WWTPs, Yang et al. (2020) found that the sludge dewatering room, with
an annual average concentration of 2150 CFU/m3, is the reactor that
produces the most total bacteria in aerosols, followed by the aerated
tank (2043 CFU/m3), pre-anoxic tank (1370 CFU/m3), and fine grid
(1193 CFU/m3). Uhrbrand et al. (2017) also found microorganisms such
as Enterococcus and Kocuria in WWTPs. Additionally, Wang et al.
(2017b) detected five ARGs, Yang et al. (2014) detected three ARGs such
Fig. 1. Publications and citations of works and articles per annum retrieved on the topic of ‘antibiotic resistance genes aerosols’ in the Web of Science from 1995
to 2021.
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Journal of Cleaner Production 348 (2022) 131094
as quinolones resistance genes and Moreira et al. (2016) detected MGEs
in WWTPs (Table 1). Aeration in wastewater treatment processes can
increase microbial activity, intensify aerosolization, and increase bio­
aerosol emissions. Additionally, high aeration shear can affect the size
distribution and morphology of activated sludge flocs and further affect
the size of bioaerosol particles discharged into the air. Disinfection
processes such as chlorination and ultraviolet treatment can also induce
the horizontal transfer of ARGs and promote transmission (Su et al.,
2014), which explains—to some extent—why the concentrations of
bioaerosols detected in different reactors differ. Additionally, Yang et al.
(2020) found that the components of wastewater also affect the emission
of bioaerosols because the atomization ability of different dominant
bacteria differs. Gaviria-Figueroa et al. (2019) found that the wind di­
rection was also a factor affecting bioaerosol concentration. If bio­
aerosols containing ARGs are not controlled in the process of wastewater
treatment, they will cause ARG pollution to the air around the WWTP.
In addition to the risk that the wastewater in the WWTPs can produce
bioaerosols with ARGs, airborne ARGs can also be produced in gray­
water—domestic wastewater comprising bathroom water, kitchen
water, and laundry water. High levels of heterotrophic bacteria,
Enterococcus spp., Staphylococcus spp., Klebsiella pneumoniae, Escherichia
coli, and Pseudomonas spp. Usually accumulate near graywater-
treatment systems and easily produce bioaerosols (Benami et al.,
2016a). The bioaerosols may carry many ARGs and pathogens and cause
infection upon inhalation, ingestion, or skin contact. E. coli and Entero­
cocci, as well as pathogens, increase when graywater is stored for several
hours or more (Birks and Hills, 2007). More seriously, when graywater
or effluent from the WWTP is discharged into the surface, it pollutes the
surface water, further penetrates the soil, and pollutes the soil and
groundwater. Katukiza et al. (2015) detected 2.05 × 107 cfu (100 mL)− 1
Escherichia coli and 7.32 × 106 cfu (100 mL)− 1 Salmonella spp. In gray­
water, which demonstrated the high risk of releasing bioaerosols con­
taining ARGs in graywater. Additionally, graywater used for farmland
irrigation can transfer ARGs into crops. The increase in ARGs in water,
soil, and crops also increases the amount of ARGs that volatilize into the
atmosphere, increasing the likelihood of contact with the human body
and thus endangering it.
2.2. Municipal solid waste landfill
Similar to the WWTP, which is the concentration of urban sewage,
landfills are the hotspots of urban solid waste. An estimate is that by
2030, the production of global solid waste will reach 2.6 billion metric
P. Chen et al. Journal of Cleaner Production 348 (2022) 131094

Fig. 2. The abundance of ARGs detected in bioaerosols from different sources. (a) ARGs in bioaerosols from livestock farms and WWTPs: CF-A=Chicken farm total
suspended particles, CF=Chicken feces, PF-A=Pig farm total suspended particles, PF=Pig feces, WWTP-A = WWTP total suspended particles (Adapted from Ref
(Yang et al., 2018). with permission from RightsLink/Elsevier); (b) ARGs in bioaerosols produced by pork, chicken and fish after 1–10 days of fermentation in
landfills (Quoted from Ref (Yu et al., 2021). with permission from RightsLink/Elsevier); (c) ARGs in bioaerosols from living area of Beijing and Shijiangzhuang in
China (Quoted from Ref (Zhang et al., 2019). with permission from RightsLink/Elsevier); (d) ARGs in bioaerosols from urban hospital (Gao et al., 2018b) with
permission from RightsLink/Elsevier).

tonnes (Yang et al., 2021). The massive production of waste increases
the load of municipal solid waste (MSW) landfills and increases the
difficulty of waste treatment. Additionally, types of solid waste,
including domestic garbage, medical waste, and agricultural waste, and
harmful byproducts in leachate (Iskander et al., 2020) increase the
complexity of the composition of pollutants in landfills and provide a
more favorable environment for antimicrobial resistance microbes
(Wang et al., 2020a). At a landfill in Guangzhou, China, which produces
6500 tons of garbage per day, Zhang et al. (2016) found tetracycline,
sulfonamide, ampC β-lactamase resistance genes, and integrons. Ac­
cording to Li et al. (2020), the β-lactamase resistance gene, blaTEM-1
originating from MSW treatment system, was inhaled about
106–107copies/day by landfill workers, seriously endangering their
health. Additionally, Yu et al. (2016) detected MGEs, including inte­
grons, insertion sequences, plasmids, and transposons at the Shanghai
landfill in China, which contribute to airborne ARG transmission and
cause harm to surrounding residents. Zhang et al. (2016), Chen et al.
(2019), Wang et al. (2020a) and Yu et al. (2021) (Table 1) also found
different microorganisms (e.g., Firmicutes, Bacteroidetes, and Bacilli) and
various ARGs (e.g., ermB, ermF, tetB, and sul2) in different landfills,
suggesting the prevalence of microorganisms and ARGs in landfills.
Notably, microplastics account for approximately 20% of the MSW
dumped and can promote the accumulation of ARGs as vectors of ARB
and ARGs (Su et al., 2021). The size of microplastics is from 100 nm to 5
mm, which provides a rich specific surface area for adsorption of pol­
lutants and microbial growth (Alfaro-Núñez et al., 2021). The organic
matters absorbed on the surface of microplastics also provide nutrition
for microorganisms and further promote the formation of a stable bio­
film (Wu et al., 2019). The biofilms, as a whole robust community on the
plastic have high cooperative behaviors and diversity, which is
conductive to improving the resilience to perturbation and the capacity
of maintaining the activities of the biofilm members (Philippot et al.,
2013). Hence, the stable biofilms can produce, carry abundant ARGs and
affect the composition of ARGs continuously (Yang et al., 2019). Wang
et al. (2020b) found various ARGs, which mainly included tetM, tetS, and
tetW. Wu et al. (2019) also reported many types of ARGs, including the
multidrug resistance gene smeE, mdsC, fluoroquinolone resistance gene
qnrVC6, MLS resistance gene ermF, lnuE (0.023%), and beta-lactam
resistance gene blaVEB-9 (0.024%), which demonstrated the enrich­
ment of ARGs by microplastics. Additionally, they also found abundant
integron-integrase gene classes 1 and 2, which are MGEs that promote
horizontal transfer of ARGs, suggesting the important role of micro­
plastics in promoting ARG transfer. Unfortunately, the microplastic with
ARGs can be accumulated along with the food chain due to predation
and eventually enter the human body, endangering human health (Tang
et al., 2021). Notably, coronavirus disease 2019 (COVID-19), has led to a
sharp increase in plastic production worldwide. For example, the
average generation rate of plastic waste in Southeast Asian countries
increased by 800 t per day after the COVID-19 pandemic (Haque et al.,
2021). According to Watson et al. (2015), the total output of plastics will
reach 33 billion tons by 2050; thus, the effect of ARG enrichment and
propagation in microplastics will last for thousands of years. As a crucial
part of ARG enrichment in solid waste in landfills, microplastics will
increase the probability of ARGs entering the air and thus corresponding
methods should be studied to reduce the risk of airborne ARG propa­
gation and mitigate the resulting ARG pollution.
2.3. Livestock farm and composting facilities
In animal husbandry, antibiotics have been used to increase the

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P. Chen et al. Journal of Cleaner Production 348 (2022) 131094

Table 1
Sources of ARGs in bioaerosols.
Sources Bacterial community and quantity ARGs and MGEs References

WWTPs ● Acinetobacter, Arcobacter, Pseudomonas, Aeromonas, Bacteroides, Prevotella, – Yang et al.

Enterobacter, Escherichia-Shigella, Stenotrophomonas 1193 CFU/m3–2043 CFU/ (2020)
m3
● Enterococcus, Kocuria, Micrococcus, Staphylococcus, Streptomyces, Arthrobacter, – (Uhrbrand et al.,
Bacillus, Cellulosimicrobium, Dietzia, Microcbacterium, Rhodococcus, 2017)
Sphingomonas, Agrococcus, Solibacillus
– ● Quinolones, chloramphenicol, tetracycline, Wang et al.
aminoglycosides, sulfonamides resistance genes (2017b)
– ● Sul1, qnrS, blaTEM, intI1 Moreira et al.
(2016)
– ● Quinolone, sulfonamide, tetracycline resistance Yang et al.
genes (2014)
Graywater ● Enterococcus spp., Staphylococcus spp., Klebsiella pneumoniae, Escherichia coli, – Benami et al.
Pseudomonas spp. (2016a)
● Escherichia coli 2.05 × 107 cfu (100 mL)− 1 Salmonella spp. 7.32 × 106 cfu (100 – Katukiza et al.
mL)− 1 (2015)
● Campylobacter, Salmonella – Birks and Hills
(2007)
Municipal Solid – ● AmpC β-lactamase, tetB, sul2, tetA, tetX, intI1 Zhang et al.
Waste (2016)
– ● Tetracycline, β lactams, sulfonamide, Chen et al.
fluoroquinolone, macrolide resistance genes, class- (2019)
1 integrons
● Firmicutes, Bacteroidetes, Synergistetes, Proteobacteria, Chloroflexi ● Tetracycline, multidrug, vancomycin, beta- Wang et al.
lactams, sulfonamide, aminoglycoside resistance (2020a)
genes
– ● Sulfonamides, sul-I, sul-II and sul-III, plasmids, Yu et al. (2016)
transposons, integrons, insertion sequences
● Acidobacteria, Actinobacteria, Deinococcus-Thermus Nitrospirae, Proteobacteria ● TetM, tetS, tetW 7.9 × 10− 3 to 5.7 × 10− 2 copies/ Wang et al.
16 S rRNA (2020b)
● Chlorobi, Acidobacteria, Gemmatimonadetes, Actinobacteria, Fibrobacteres, ● SmeE, mdsC, qnrVC6, ermF, lnuE, blaVEB-9, Wu et al. (2019)
Planctomycetes, Hydrogenedentes, Chlamydiae aadA13, fosK, cmx, dfrA15
● Bacilli, Burkholderia-Paraburkholderia, Mycobacterium ● ErmB, ermF, tetM, tetA, tetO, sul2, mexF, acrF Yu et al. (2021)
Livestock farm ● Firmicutes, Bacteroidetes ● TetB, tetL, tetM, tetO, tetQ, tetW McEachran et al.
(2015)
● Corynebacterium ● Chloramphenicol, sulfonamide, vancomycin, Yang et al.
polymyxin, tetracycline, trimethoprim resistance (2018)
genes
● Staphylococcus aureus, Salmonella spp., fecal coliforms ● Ampicillin, erythromycin, oxytetracycline, Gibbs et al.
penicillin, tetracycline, tylosin resistance genes (2004)
● C. perfringens, Enterococcus, E. coli, Campylobacter ● TetA, tetC, tetG (Létourneau
et al., 2010)
Composting ● Bacilli, Actinobacteria – Ferguson et al.
facilities (2021)
● Firmicutes, Actinobacteria, Acidobacteria, and Proteobacteria ● Vancomycin, betalactams, tetracycline resistance Xiao et al.
genes, transposase genes, and integrase genes (2021)
● Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes ● Sul1, sul2, sul3, sulA, and intI1 Lin et al. (2021)
Medical – ● Quinolones, aminoglycosides, sulfonamides, third- Wu et al. (2020)
industry generation cephalospontibiotics resistance genes
● Massilia, Sphingomonas, Methylobacterium, Methylophilus, Micrococcineae, ● MecA genes, blaCTX-M Gao et al.
Corynebacterineae (2018b)
● S. maltophilia, Enterobacter cloacae, Chryseobacterium sp., S. paucimobilis ● TetG, ermF, ermX Gilbert et al.
(2010)
● Methicillin-resistant Staphylococcus aureus, coagulase-negative staphylococci ● Aac(6′ )-aph(2′′ ), ermA, mecA, vanA Drudge et al.
(2012)
Natural ● Pseudomonas, cladosporium, methylobacterium, friedmanniella, rosenbergiella – Manirajan et al.
environment (2018)
● Anamorphic, ascomycetes, basidiospores – Camacho et al.
(2018)
● Pseudomonas, Alternaria, Bacilli, Defluviicoccus – Wei et al.
(2019b)
● Bradyrhizobium, Methylobacterium, Stenotrophomonas Tanaka et al.
(2019)
● Methylobacterium, Rhodoplanes, Flavobacterium, Streptococcus – Michaud et al.
(2018)

4
P. Chen et al.
growth rate of animals. Therefore, many ARGs have been identified in
livestock farms, especially in animal feces. Many microorganisms such
as Firmicutes, Corynebacterium, Staphylococcus aureus and C. perfringens
(Létourneau et al., 2010) and ARGs such as tetracycline resistance genes
(McEachran et al., 2015), chloramphenicol resistance genes (Yang et al.,
2018) and ampicillin resistance genes (Gibbs et al., 2004) (Table 1) were
reported in livestock farms. Additionally, Liu et al. (2012) demonstrated
that for some strains isolated from feces, indoor and outdoor air had the
same antibiotic resistance, and strains with the same REP-PCR trace
identification result carried the same type of ARGs, indicating that an­
imal feces are probably a major source of airborne ARGs on livestock
farms. Karkman et al. (2019) also agreed that the presence of ARGs is
largely due to fecal contamination. The literature reported that each
cattle or pig can produce hundreds to thousands of kilograms of manure
and urine, and that each chicken or duck can generate approximately 30
kg of manure over their lifespans (Hu et al., 2017), which undoubtedly
cause serious ARG pollution in the air. In addition to the direct release of
bioaerosols containing ARGs from animal feces, the treating process of
animal feces can also release ARGs in bioaerosols.
Composting, which produces nutrient rich fertilizer, is widely used to
treat animal manure, sludge or other solid wastes through regulating
environment conditions such as moisture, carbon nitrogen ratio, venti­
lation volume and material particle size (Douglas et al., 2017). However,
it is demonstrated that composting generated bioaerosols, particularly
during aeration and stirring activities, causing air pollution and
threatening human health (Gao et al., 2018a). Ferguson et al. (2021)
detected abundant Actinobacteria, which could carry ARGs and MGEs,
and sensitizers such as endotoxins at an open windrow green waste
composing site, suggesting the airborne ARGs pollution and the risk of
human health related to composting facilities. Furthermore, the fertil­
izer produced by composting continues to produce microbial aerosols
containing ARGs and pollutes the soil. For example, Xiao et al. (2021)
detected a total of 249 ARGs and 12 MGEs in soil-plant systems with
waste sludge compost. Lin et al. (2021) also found industrial thermo­
philic manure composting produced ARGs such as sul1 and sul2 although
it removed most of the antibiotic residues. Notably, although high
temperature during thermophilic composting can kill pathogen and
reduce ARGs, ARGs typically rebound during the mature phase of
composting because of a significant resurgence of ARB at low temper­
atures (Liao et al., 2018). Hence, optimizing composting to decrease the
dissemination of antibiotic resistance and reduce pollution of bio­
aerosols containing ARGs is necessary. Cui et al. (2020) designed a
semi-permeable membrane-covered thermophilic composting to pre­
vent bioaerosols in the air from entering the composting system,
reducing ARGs and MGEs in fertilizer. Awasthi et al. (2019) demon­
strated that adding an appropriate amount of clay affected the distri­
bution ARB and reduced ARGs in the compost, which is beneficial to
reduce airborne ARGs in bioaerosols produced in the composting pro­
cess and fertilizer, and further mitigate the ARGs pollution in the air and
soil. However, the reduction effect of ARGs is not enough to eliminate
threats to human health and needs further research.
2.4. Medical industry
ARGs generated by the medical industry require attention because
the medical industry often uses many antibiotics to treat diseases. Wu
et al. (2020) found that the sample of isolated E. coli from three wards
was resistant to quinolones, aminoglycosides, sulfonamides, and
third-generation cephalosporin antibiotics, which can be inhaled by
patients and medical staff and directly threaten to their health. They also
demonstrated that ARGs can be transmitted from wards to corridors and
even around hospitals through gas exchange, posing a health threat to
nearby residents by homology analysis with pulsed-field gel electro­
phoresis. Gao et al. (2018b) obtained similar conclusions through the
detection of bioaerosols in five hospitals. They found multiple antibiotic
resistance genes such as mecA genes and ARGs related to horizontal gene
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Journal of Cleaner Production 348 (2022) 131094
transfer (HGT) such as blaCTX-M, which aggravate ARG dissemination in
the air. Gilbert et al. (2010) and Drudge et al. (2012) also detected
microorganisms (e.g., S. maltophilia, Enterobacter, and
Methicillin-resistant Staphylococcus aureus) and ARGs (e.g., tetG, ermF,
ermA, and mecA) in hospitals (Table 1), demonstrating that hospitals are
one of the important sources of bioaerosols with ARGs. Additionally,
temperature, humidity, season, location, and moisture in the air could
affect the microbial species and the ARGs they carried. The microor­
ganisms in dust could also spread into bioaerosols. Therefore, in addi­
tion to controlling bioaerosols in hospitals, the environmental
conditions and dust in hospitals should also be considered to reduce the
generation and transmission of ARGs in the air.
Additionally, the prevalence of COVID-19 has increased the use of
antibiotic significantly such as amoxicillin (Mohamad et al., 2022),
which may potentially aggravate ARGs contamination (Pulia et al.,
2020). It was reported that 72% of hospitalized COVID-19 patients
received antibiotics and the prescription rates of broad-spectrum anti­
biotic agents was high (Rawson et al., 2020), which increases the risk of
inducing ARGs. Kang et al. (2022) detected 405 ARGs such as mexF and
mexD in the fecal samples from patients with community-acquired
pneumonia, which is 98 more than the fecal samples from anti­
biotics-naïve COVID-19 patients. As mentioned in Section 2.2, the
accumulation of microplastics produced by disposable medical supplies
during COVID-19’s popularity also can increase the risk of the genera­
tion and transmission of airborne ARGs. Hence, the effect of COVID-19
on airborne ARGs need to be valued and further studied.
2.5. Natural environment
Some ARGs in the atmosphere are caused by human activity, and the
other ARGs are caused by natural conditions such as sea spray, plant
pollination, volcanic eruption, and wildfires (Ruiz-Gil et al., 2020).
According to Michaud et al. (2018), microorganisms in seawater have a
high aerosolization capacity that can enter the air through wave
breaking and bubble bursting, becoming a part of bioaerosols. With the
movement of ocean currents and air, these microorganisms can spread
to other land or water environments, causing a wide range of pollution.
Pollination is also a source of bioaerosols. In pollen-related microbial
populations, Firmicutes, Actinobacteria and Proteobacteria are the most
abundant bacterial phyla (Manirajan et al., 2018), which are related to
Methylobacterium. The features of Methylobacterium including
nitrogen-fixing activity, pigmentation, biofilm formation, facultative
methylotrophy, and desiccation tolerance, make it easy to survive in the
atmosphere. In volcanic eruptions, microorganisms are released, and the
ARGs they carry are further propagated in the air. Additionally, volcanic
ash can react with other substances to generate organics and be used by
microorganisms (Ruiz-Gil et al., 2020), which promotes the transfer of
microorganisms and may expand the scope of ARG pollution. Near the
mountain, aerosols carrying different microorganisms are distributed in
different particle sizes (Wei et al., 2019a). In wildfires, microorganisms
on leaf surfaces and soils are aerosolized and spread by smoke produc­
tion. Microorganisms in bioaerosols (e.g., Bradyrhizobium) have also
been found at high-altitude and suburban sites with less human activity
(Tanaka et al., 2019). In Madeira Island in the North Atlantic, Camacho
et al. (2018) found an increase in fungal spores after an urban or forest
fire occurrence, which increased the risk of ARG transmission and
showed that even without human activities, bioaerosols and ARGs were
also released.
3. Transmission and harm of ARGs in bioaerosols
3.1. Propagation of microorganisms carrying ARGs in the atmosphere
ARGs are not only propagated in a particular area or even spread on a
global scale. They can be transmitted not only through water, but also
directly to humans through food. However, only the propagation of
P. Chen et al.
ARGs in biological aerosols is mainly introduced in this review.
Anthropogenic activities, such as aeration and stirring in sewage treat­
ment processes, clinical treatment, and disposal of solid waste, cause
ARB to become aerosols and directly lead to ARG accumulation in the
air. Some natural phenomena, mainly including plant pollination, vol­
canic eruption, wildfires, wave breaking, and bubbles bursting on the
ocean surface (as mentioned in Section 2) also contribute to the increase
in ARGs in bioaerosols. The microbial aerosols produced by the rupture
of ocean waves causes ARGs to spread from the marine environment to
the air and are transferred from the ocean to the land with the migration
of waves (Fig. 3) (Ruiz-Gil et al., 2020).
Bioaerosols carrying ARGs suspended in the air can move under the
push of the wind and dust plume, making them dispersed in various
corners. Jeon et al. (2011) have demonstrated a surge in microbial
concentration during dust events, which often occurs in arid areas in
South America and Australia. A more serious phenomenon is that dust
mobilization also enriches microorganisms from other environments,
which increases the risk of ARGs. Additionally, airborne bacteria tend to
adhere to other particles to form larger particles on other particles
because by doing this, their ability to cope with the pressure from the
environment and promote molecular communication improves. Coarse
particles can carry more microorganisms than fine particles can, and this
percentage can reach approximately 80% in terms the diversity and
relative abundance of bacteria (Bowers et al., 2013). However, fine
particles can remain in the air for more time because of the advantage of
a small volume than coarse particles, which can easily cause more sus­
tained ARG contamination (Smith et al., 2018). In addition to time
persistence, microbial aerosols in the air can also be transported over a
wide range because of their strong tolerance to the environment, causing
bioaerosols in the atmosphere to aggravate ARG pollution in time and
space.
Heavy rainfall is also an important driver for the transmission of
ARGs in the bioaerosols. Rainfall can increase humidity and airborne
bacterial diversity and is conducive to the survival of airborne bacteria
(Dong et al., 2016). According to Joung et al. (2017), every raindrop
contains bacteria such as Pseudomonas syringae, Bacillus subtilis and
Corynebacterium glutamicum and can generate over 100 bioaerosol
droplets smaller than 10 μm. Notably, rainfall can increase the survival
rate of microorganisms, which in turn increase rainfall. For example,
Fig. 3. Transmission of ARGs in bioaerosols.
6
Journal of Cleaner Production 348 (2022) 131094
rainfall increases the potential ice- and cloud-nucleating bacteria such as
Pseudomonas, which can in turn induce rainfall for up to approximately
20 days, increasing the aerosol of microorganisms and survival time of
microorganisms in the air (Bigg et al., 2015). Hence, the interaction
between rainfall and ARGs in bioaerosols deserves further study to
minimize the ARGs pollution in the air. However, not all rainfall in­
creases bioaerosol concentration and aggravates ARG pollution.
Generally, rainfall with low intensity can aggravate particle deposition
in the air, resulting in its settlement into the soil or falling on the plant
surface, reducing its suspension concentration (Uetake et al., 2019).
However, after sunny weather, microorganisms containing ARGs on the
soil and plant surface may be re-released into the atmosphere. ARGs can
be propagated between species, along with the impact of human activ­
ities (e.g., migration and tourism) and natural phenomena (e.g., tsunami
and rainfall), such that ARGs spread globally (Hernando-Amado et al.,
2019), indicating that investigating the spread of ARGs in bioaerosols is
significant in controlling ARG transmission worldwide.
3.2. Hazard of bioaerosols carrying ARGs
ARGs carried by ARB can make drugs ineffective in treating life-
threatening diseases and further endanger the life and safety of
humans and animals (Jiang et al., 2013). An estimate indicated that the
number of deaths caused by ARB will increase to 10 million by 2050
(Posada-Perlaza et al., 2019). ARGs in bioaerosols can be obtained by
direct inhalation and food intake, such as vegetables deposited with
microbial aerosols. Especially in hospitals, patients are exposed to an
environment containing bioaerosols carrying ARGs for a long time,
which is not conducive to the healing of patients. More seriously, ARGs
can accumulate and spread continuously, especially from the air to the
ground with rainfall, and then spread to animals, plants, or water bodies
and finally into the human body through the food chain. Moreover, once
livestock or crops obtain ARGs, the use of antibiotics will be increased to
resist drug resistance, causing a vicious circle of antibiotic and ARG
pollution. Multiple ARGs are also a very thorny problem that has
attracted attention worldwide.
Additionally, the countless fungi and bacteria in bioaerosols can lead
to diseases induced by stimulation, allergies and infections via inhala­
tion, ingestion, or skin contact with bioaerosols (Kim et al., 2018). Wang
P. Chen et al. Journal of Cleaner Production 348 (2022) 131094

et al. (2019a) showed that bioaerosols penetrated the pulmonary system
and might accelerate their propagation in a highly dynamic atmospheric
environment. Specific diseases related to biological aerosols include
toxic allergies, gastrointestinal symptoms, respiratory diseases, infec­
tious diseases and cancers, especially respiratory diseases (Nair, 2021).
For example, a fungus found in the residence of asthmatic children may
be related to asthma diseases (Mousavi et al., 2016). More seriously,
fungi also produce airborne spores, conidia, hyphae, and other frag­
ments, further expanding their impact range. Components of the bac­
terial cell wall, such as endotoxins and peptidoglycans, may also lead to
respiratory diseases (Douwes et al., 2003). Some bacteria in bioaerosols
can freeze plants and damage cells in plant tissues (Cid et al., 2016).
4. Composite contamination of ARGs in bioaerosols
Composite contamination, especially compound pollution of metals
and ARGs is crucial to aggravate airborne ARG pollution although it is
often ignored by researchers. Similar to antibiotics, metals and PAHs
have a wide range of sources and may play a selective role in antibiotic
resistance.
4.1. Compound contamination of ARGs and MRGs
According to Warnes et al. (2012), antibiotics and metals may be the
main drivers of antimicrobial resistance. Metals, similar to antibiotics,
have many sources, for example, the medical industry, animal hus­
bandry, and MSW landfills (Zhou et al., 2020). In a hospital, Gullberg
et al. (2014) reported the contribution of low concentrations of heavy
metals and antibiotics to extended spectrum β-lactamase (ESBL)
encoding plasmid (220 Kbp) maintenance, which is resistant to six an­
tibiotics (e.g., tetracycline) and three heavy metals: copper, arsenic, and
silver. Deredjian et al. (2011) also reported a multiresistance phenotype
and the promotion of antibiotic exposure on the selection of ARB and the
maintenance of antibiotic resistance in hospital. In animal husbandry,
the use of many antibiotics is accompanied by the use of metals as
supplementary feed for animals to promote growth, treat infectious
diseases, and prevent infection (Zhao et al., 2021). However, animals
neither absorb or transform most of the metals they consume; thus, these
metals are discharged with feces, and the heavy metals in feces are
further aerosolized and diffused into the air, causing pollution (Hu et al.,
2017). Gomez-Sanz et al. (2013), Feβlera et al. (2016) and Falgenhauer
et al. (2015) all detected the co-resistance genes of antibiotics and
metals in livestock farms, indicating the general existence of composite
pollution of metal and antibiotics in animal husbandry. Interestingly, all
of the compound resistance detected by them included copper resis­
tance, which might indicate that copper is one of the most common
metal additives in animal husbandry and played an important role in
promoting the generation and transmission of airborne ARGs (Table 2).
As the hotspot of solid waste, landfills are inevitably polluted by the
combination of antibiotic resistance and heavy metal resistance. In
China, Wang et al. (2019a) found 14 antibiotics and 11 types of metal in
three landfills, with total contents ranging from 157.22 to 1752.01
μg/kg and 19,624.62–30,624.01 mg/kg, respectively. Wu et al. (2015)
found five antibiotics (e.g., sulfonamide) and seven types of metals (e.g.,
lead) in Hulin and Xupu transfer stations and a landfill reservoir,
Shanghai. Yu et al. (2016) also found MGEs including plasmids, trans­
posons, integrons, and insertion sequences, which demonstrated the
universality and hazard of composite contamination of antibiotic resis­
tance and metal resistance in landfills. Additionally, metals and antibi­
otics that infiltrate the soil may enter the atmosphere through
aerosolization, causing cardiovascular diseases (Si et al., 2019), which
can aggravate ARG pollution in the air. Therefore, researchers should
not only pay attention to the traditional soil pollution and leachate
leakage problems in landfills, but also pay attention to compound
pollution of airborne ARGs. In addition to the places affected by human
activities, the co-selection of antibiotic resistance and metal resistance
has also been found in natural environments (Table 2). In the river,
Vancomycin, teicoplanin resistance genes, and six MRGs (As, Cd, Cr, Cu,
Hg, and Pb resistance genes) were detected, which severely damaged the
quality of water and their resources and produced high risk to the
associated life forms (Rahman and Sing, 2018). In the marine environ­
ment, Osman et al. (2010) found co-selection between zinc and antibi­
otics, including ampicillin, streptomycin, tetracycline, kanamycin, and
penicillin, on the pMA22 plasmid in Halomonas. Similarly, Cd, Cu, and
erythromycin resistance genes were found in coastal marine sediment
(Table 2). In Antarctic waters with a pristine environment, De Souza
et al. (2006) detected co-selection between penicillin, Cu, ampicillin,
and Ni, which proved that co-selection of metals and antibiotics is
ubiquitous.
ARGs and metals can be co selected because they have similar
resistance mechanisms. For antibiotics, there are six main resistance
mechanisms: the formation of antibiotic efflux pumps, the decrease in
membrane permeability, antibiotic inactivation, biofilm formation,
mutation of genes encoding the target of antibiotics, and extracellular
sequestration (Imran et al., 2019)—some of which can also resist metals.
Co-selection resistance mechanisms of antibiotics and metals can be
divided into co-resistance, cross-resistance, and co-regulatory resistance
mechanisms (Fig. 4). Co-resistance occurs when two or more resistance

Table 2
Compound contamination of ARGs and MRGs.
Sources Metal or MRGs ARGs References

Municipal solid ● Co, Pb, As, Cr, and Cu resistance ● Sulfonamides, sul-I, sul-II, sul-III, plasmids, transposons, integrons, insertion Yu et al. (2016)
waste genes sequences
● Cu, Cr, Pb, Cd, As ● Sul1, ermB, sul2, ermB, mexF Wang et al. (2019a)
● Cd, Cr, Ni, Pb, Zn, Cu, As ● Sul1, sul2, tetQ, tetM, ermB, mefA Wu et al. (2015)
Medical industry ● Si, Cu, and As resistance genes ● Aminoglycosides, β-lactams, tetracycline, macrolides, trimethoprim, sulfonamide Gullberg et al. (2014)
resistance genes
● Cu, and Hg resistance genes ● Minocycline and trimethoprim sulfamethoxazole resistance genes Deredjian et al. (2011)
Natural ● As, Cd, Cr, Cu, Hg, and Pb resistance ● Vancomycin, teicoplanin resistance genes Rahman and Sing
environment genes (2018)
● Zn resistance gene ● Ampicillin, streptomycin, tetracycline, kanamycin, and penicillin resistance genes Osman et al. (2010)
● Cu, and Ni resistance genes ● Penicillin, and ampicillin resistance genes De Souza et al. (2006)
● As, Cu, and Zn resistance genes ● Penicillin, ampicillin resistance genes Farias et al. (2015)
● Cd, and Cu resistance genes ● Erythromycin resistance genes Vignaroli et al. (2018)
● Cu, and Zn resistance genes ● Tetracycline resistance genes Flach et al. (2017)
● Cu, and Hg resistance genes, mco, ● ErmT, tetL, dfrK, ermC Gomez-Sanz et al.
copA (2013)
Animal husbandry ● Cu, and Cd resistance genes, copA, ● AadD, ermB, dfrK, tetL, apmA Feβlera et al. (2016)
mco
● Cu resistance genes, silABC, pcoS, ● BlaACC-1, blaVIM-1, aacA4, aadA1, strAB, sul1 Falgenhauer et al.
pcoE (2015)

7
P. Chen et al.
genes are on the same MGEs, including plasmids, integrons, and trans­
posons (Pal et al., 2017). Parkhill et al. (2001) reported multiple ARGs,
such as ampicillin resistance genes and mercury resistance, on a con­
jugative plasmid (pHCM1) of Salmonella enterica typhi CT18. Farias et al.
(2015) also found antibiotic resistance (β-lactams and fluoroquinolones)
and five metal resistance (cobalt, zinc, cadmium, chromium, and cop­
per) in three plasmids of bacterial isolates. Moreover, the presence of
metals can also increase the enrichment of MGE and increase the
abundance of ARGs (Poole, 2017). Notably, class I integrons can cata­
lyze the co-selection process, aggravating ARG pollution (Imran et al.,
2019). Cross resistance refers to antibiotics and metals that have the
same resistance mechanism, which contains various mechanisms such as
efflux pumps, biofilms, and extracellular sequestration related to
extracellular polymeric substances (EPS). Mata et al. (2000) reported a
multiple-drug resistance efflux pump in gram-positive Listeria mono­
cytogenes with resistance to zinc, cobalt, and cadmium, and multiple
antibiotics (clindamycin, erythromycin, and josamycin) can expel them
out of cells. In Burkholderia cepaceae, the formation of the DsBA-DsbB
disulfide bond makes cells resistant to antibiotics and heavy metals
(Hayashi et al., 2000). In Enterobacter cloacae strain P2B, microorgan­
isms become resistant to Pb+2 ions and antibiotics such as oleondamycin
through an extracellular sequestration mechanism (Naik et al., 2012).
A. haemolyticus MMC 8 can resist AgNO3, HgC12, and 14 antibiotics by
forming biofilms (Gaidhani et al., 2014). Co-regulatory resistance is less
reported than co-resistance and cross resistance. For example, when
exposed to zinc, isolates of Pseudomonas aeruginosa develop resistance by
activating CzcCBA and deactivating oprD, which are transcriptionally
linked, resist antibiotics and metals via operons (Baker-Austin et al.,
2006). The co-selection mechanism of metals and antibiotics may in­
crease the risk of exposure and transmission through the HGT of ARGs to
the air and eventually harm the human body (Hernando-Amado et al.,
2019).
Fig. 4. Co-resistance mechanism of ARGs and MRGs. (a) Co-resistance of antibiotics and metals, which is mainly related to MGEs (e.g., integrons, plasmids, and
transposons); (b) Cross resistance of antibiotics and metals, mainly including efflux pumps and EPS generated by cells; (c) Co-regulation of antibiotics and metals
which is related to the expression of the efflux pump and ARGs and MRGs.
8
Journal of Cleaner Production 348 (2022) 131094
4.2. Compound contamination of polyaromatic hydrocarbons (PAHs)
and antibiotics
Similar to metals, PAHs can also form compound pollution with
antibiotics (Table 3). The mechanism of co-selection between PAHs and
antibiotics is mainly efflux pumps, which is similar to the mechanism of
that between metals and antibiotics. The difference between the two
types of compound pollution is that this efflux pump gene is located on
chromosomes rather than plasmids (Gorovtsov et al., 2018). In the case
of triple compound pollution of antibiotics, PAHs and metals, the situ­
ation may increase in complexity and seriousness. The co-pollution of
PAHs and antibiotics in soil has been widely reported and attracted
attention. Chen et al. (2017) reported the compound contamination of
PAHs (e.g., naphthalene) and antibiotics (e.g., aminoglycosides) in the
soil near petrochemical plant and demonstrated the enrichment of ARGs
by PAHs. Sun et al. (2015) detected the compound contamination of
phenanthrene, roxithromycine and sulfadiazine in the soil of livestock
farms. Sazykin et al. (2021) and Stancu and Grifoll (2011) also
demonstrated the positive relationship of polycyclic aromatic hydro­
carbon pollution and antibiotic pollution in the soil in technogenically
polluted sites, MSW landfills, rural settlements and oily sludge, respec­
tively. Furthermore, the co-resistance of PAH and antibiotics were
detected in many strains (Said et al., 2008) and in Pseudomonas fluo­
rescens strains, plasmids that transmitting ARGs and PAH resistance
genes were also found, which might increase the risk of ARG transfer
(Wang et al., 2017a). Although PAH pollution, which can change the
microbial community structure, is reported more in soil than in air, PAH
accumulation in soil is also atomized to enter the atmosphere to a certain
extent and pollute the environment. Wei et al. (2021) determined that
the average concentrations (gaseous and particulate) of PAHs in the air
from urban and rural areas of four climate zones in China was 995 ±
635 ng m− 3 in autumn, which indicates high PAH pollution in the at­
mosphere. Notably, in addition to the PAHs in the soil entering the air
through atomization, the PAHs in the air can also input to the soil
through dry or wet deposition of aerosol particles or residues of
P. Chen et al.
Table 3
Compound contamination of ARGs and PAHs.
Sources PAHs
Soil ● Naphthalene, Dibenzofuran, Acenaphthylene, Acenaphthene,
Fluorene, Phenanthrene, Fluoranthene, Pyrene
● Phenanthrene
● Naphthalene, biphenyl, fluorene, phenanthrene, anthracene,
fluoranthene, pyrene
Oily ● Naphthalene, 2-methylnaphthalene, fluorene
sludge
Strains ● Toluene, phenanthrene, anthracene, fluoranthene, naphthalene
● Pyrene, fluoranthene, phenanthrene
Coastal ● Naphthalene, phenanthrene
water
vegetative litter and by processes of air− soil partitioning (Nam et al.,
2008). Therefore, to reduce the compound contamination of airborne
ARGs with PAHs, the PAHs in soil also need to be paid attention to due to
their indiscerptible relationship with airborne PAHs. Bosch et al. (2015)
reported that 75 ± 6% of PAHs in soils in the Czech Republic came from
coal combustion, which demonstrated that coal pyrolysis was the main
source of PAHs. Additionally, coal is the second largest energy source
worldwide (Adebayo et al., 2021). Hence, developing the advanced coal
combustion technology such as coal gasification and microwave pyrol­
ysis (Jiang et al., 2020) is conductive to reducing the emission of PAHs
and alleviating the compound pollution of PAHs and ARGs. In addition
to the co resistance of antibiotics and PAHs in the air and soil, the
co-resistance in water (Wang et al., 2017b) also can aggravate airborne
ARG pollution and deserves attention.
5. Influencing factors of ARG pollution in bioaerosols
ARG generation and transmission in bioaerosols are affected by
Fig. 5. Factors affecting ARGs in bioaerosols. In meteorological factors, circles with overlapping parts at different levels represent that the factors of the upper level
cause the results of the lower level (For example, temperature and particle size affect abundance and diversity of microorganisms in the air).
Journal of Cleaner Production 348 (2022) 131094
ARGs References
● Aminoglycosides, beta-lactams, chloramphenicols, fluoroquinolones, Chen et al. (2017)
macrolides, polypeptides, tetracyclines resistance genes
● Roxithromycine, sulfadiazine resistance genes Sun et al. (2015)
● CTX-M, NDM, VIM, VanA, VanB, TetM, TetO (Sazykin et al.,
2021)
● Ampicillin, kanamycin resistance genes Stancu and Grifoll
(2011)
● Chloramphenicol, tetracycline, trimethoprim, streptomycin, Hearn et al.
erythromycin resistance genes (2003)
● Tetracyclin, cotrimoxazole, beta-lactamin resistance genes Said et al. (2008)
● Sull, aadA2 Wang et al.
(2017b)
many factors. In this section, main influencing factors are divided into
four categories: meteorological factors and climate change, seasonal
factors, geographic conditions and location, and epidemic virus (Fig. 5).
Although these factors discussed here are not all influencing factors,
they can still contribute to the pollution control of airborne ARGs.
5.1. Meteorological factors and climate change
Meteorological factors, including temperature, humidity, wind
speed, particle size and atmospheric pollutants, have a significant
impact on the abundance of ARGs in bioaerosols. Temperature affects
the survival time of microorganisms in the air (Zhen et al., 2017) and
further changes the microbial community structure (Liu et al., 2018).
According to Li et al. (2018), the abundance and species of bacteria vary
with temperature. Shewanella and Halomonas were dominant above 0 ◦ C,
and Klebsiella, Ralstonia, Prevotella, and Bacteroides were the dominant
bacteria below 0 ◦ C. Different microbiological species can cause atom­
ization and different ARG-carrying capacities (Yang et al., 2020).
9
P. Chen et al.
Different from temperature, which affects the microbial abundance and
microbial species, humidity affects the amount of ARGs in the air only by
affecting microbial abundance. Because moisture increases the particle
size of bioaerosols to enhance deposition, the abundance of microbes in
the atmosphere decreases, facilitating the reduction of ARGs. Addi­
tionally, aerosolization of microorganisms in wet soil becomes more
difficult, reducing the abundance of microorganisms in the air to a
certain extent (Uetake et al., 2019). Wind speed is another crucial
meteorological factor affecting microbial concentration and diversity
and can dilute bacterial concentrations in the air, especially in heavily
polluted weather (Zhen et al., 2017). However, wind also accelerates the
aerosolization of microorganisms in soil and water surfaces, which
hinders the reduction of ARG pollution in bioaerosols (Wei et al.,
2019a). Regarding the role of wind and its main role, further exploration
is necessary. Gao et al. (2015a) observed that bacterial communities in
the air are associated with particle size, and those near 2.5 and 10 μm
were the most frequently observed. Additionally, different bacteria tend
to concentrate on different particle sizes. For example, Proteobacteria, as
a type of bacterium carrying various ARGs, is dominant on both coarse
and fine particles, and Rhodobacterales are only observed on larger
particles (Gao et al., 2015a). Therefore, both particle size and relative
humidity affect the abundance of ARGs in the atmosphere. Compared
with other meteorological factors, air pollution has a greater impact on
the richness and diversity of fungi because they provide microorganisms
with energy sources, carriers, and refuges (Hu et al., 2020a). The liter­
ature has reported that haze episodes can increase bioaerosol concen­
tration and elevate some opportunistic fungi, such as Aspergillus
fumigatus (Cao et al., 2014). Zhang et al. (2019) also observed that tnpA
and intI1 increased when PM2.5 pollution was serious, indicating that air
pollution might increase the abundance of microorganisms and exac­
erbate ARG pollution.
Moreover, according to Beugnet and Chalvet-Monfray (2013), global
warming may promote the interaction and connection among microor­
ganisms, vector species, humans and animals by increasing global bio­
logical space. El Niño has also been shown to change ocean currents and
thus the intercontinental distribution of bacteria (Martinez-Urtaza et al.,
2016), which would further affect the distribution of ARGs in the air.
Therefore, airborne ARG pollution worldwide should be paid attention
to.
5.2. Seasonal factors
In different seasons, the dominant bacteria in the air are different.
The concentration of fungal spores is highest in summer and lowest in
winter (Kumar and Attri, 2016). Regarding bacteria, plant-associated
bacteria (e.g., Sphingomonadales) are dominant in warm seasons,
whereas soil-inhabiting bacteria such as Actinobacteria are prevalent in
the dry season (Franzetti et al., 2011). Burkholderiales, Actinomycetales,
Rubellimicrobium, and Paracoccus (Rhodobacterales) have also been found
to be abundant in winter and the warmer seasons, and Rhodobacterales
are dominant (Yan et al., 2018). Additionally, the amounts of nitrogen
oxide, carbon oxide, and sulfur oxide increase due to heating and
insufficient air circulation in winter, which may affect the contamina­
tion of ARGs in the atmosphere. However, bioaerosols are affected by
many factors other than seasonal factors. Hence, concluding that they
are affected by a single seasonal factor is difficult. For example, Xie et al.
(2018) showed that the difference in microbial concentration affected
by season is more obvious in rural areas than in urban areas because
rural areas have richer sources and are more unstable than urban areas.
The influence of season on the concentration of microorganisms in the
atmosphere is intertwined with various factors and continues to be
explored by researchers.
5.3. Geographic conditions and location
Many studies have reported that the diversity of microorganisms
10
Journal of Cleaner Production 348 (2022) 131094
varies with different geographical conditions and locations. The distri­
bution of dust-associated microorganisms may change vertically in
space (Hu et al., 2020a). Maki et al. (2019a) showed that the phyla
Actinobacteria, Firmicutes, Bacteroidetes, and Proteobacteria were verti­
cally mixed and prevailed at an altitude of hundreds of meters over the
Taklimakan and Gobi deserts. Maki et al. (2019b) reported the influence
of topography (land vs. sea) on air mass movement on microorganisms
in the air. They found that Alphaproteobacteria increased at the island
site, and Actinobacteria increased at the continental site, although the
change in quantity was also related to dust events. In addition to the
impact of land and sea on microorganisms, human activities affect the
diversity of bioaerosols emitted and further affect ARGs in the atmo­
sphere. According to Li et al. (2020), farmland, sewage plants, streets
and smelters seriously affected by human activities had high bioaerosol
emission levels, and the streets of Qinghai Province, which had little
industrial and agricultural activities and low population density,
exhibited low bioaerosol emission levels. Low relative humidity and
strong ultraviolet light, which can induce the inactivation of bacteria in
the air, may contribute to the low emission of bioaerosols in Qinghai
(Peccia et al., 2001). Additionally, trees can effectively reduce wind
speed, and their leaves can adhere to air particles, which can help reduce
particle resuspension (Zheng and Li, 2019). Hence, forests can reduce
the emissions of microbes to a certain extent, reducing ARG contami­
nation in the air.
5.4. Epidemic virus
The prevalence a virus may also affect the content of microbial
aerosols in the air to a certain extent. For example, the COVID 19
outbreak that started in 2020 is having a large, sustained impact on the
ARG distribution in the air. The epidemic has thus far caused the pro­
duction of solid waste to increase sharply, which is reflected in medical
supplies. Production of single-use plastic-based medical waste has
reached more than 240 tons, which is six times higher than that before
COVID-19 in hospitals in Wuhan, China (Adyel, 2020). By 2034, global
plastic waste production is expected to reach 762 million tons (Harus­
sani et al., 2022). Rapid increases in solid waste have caused serious
pollution on beaches and in water and soil (Saadat et al., 2020) and may
exacerbate the degree of aerosolization of pollutants, which is not
conducive to the control of ARGs in the air. Additionally, as mentioned
in Section 2.4, the epidemic has increased the use of antibiotics and
further promoted the generation of ARGs (Pulia et al., 2020). However,
many studies have reported that air pollution was alleviated by the
decrease in human activities after the COVID-19 outbreak (Wang and
Su, 2020), which demonstrated that the epidemic played a positive role
in alleviating air pollution to a certain extent. This positive effect is
probably only temporary, namely, once the COVID-19 decreases to a
certain extent, air pollution may worsen again (Gautam, 2020). Addi­
tionally, these studies on air pollution during the COVID-19 pandemic
were limited to inorganic substances, such as carbon monoxide and ni­
trogen dioxide and did not involve microorganisms and ARGs. There­
fore, the impact of the COVID-19 pandemic on ARGs in the air remains
unclear.
6. Challenges and outlooks
Although the exploration of ARGs is more and more in-depth, most of
the research is often devoted to the ARGs in water and soil, and there is
still very little research on the ARGs in bioaerosols. Hence, the trans­
mission of ARGs in bioaerosols is still not very clear and there are many
challenges, such as how to monitor ARGs in bioaerosols, control their
transmission, assess exposure risk, which need to be solved in future
research.
P. Chen et al.
6.1. Challenges of control ARGs in bioaerosols
(1) The detection of ARGs in bioaerosols, including the collection of
bioaerosols and detection of ARGs, is very important for the
research and control of ARGs in the air. Although some studies
have reported the methods of collecting bioaerosols such as
impaction, impingement, filtration, gravitational settling, elec­
trostatic precipitation, and cyclone separation (King et al., 2020),
the detection is affected by many factors such as location, time,
temperature and ultraviolet radiation (Douglas et al., 2017),
which impact on viability of bioaerosols and make the results lack
of accuracy and reliability. Specially, the size distributions of
particles are related to the distribution of biological species in
bioaerosols (Ferguson et al., 2021). Hence, the methods such as
ultraviolet light-induced fluorescence (UV-LIF) based methods
(Feeney et al., 2018), which can characterise size fractionated
bioaerosol emissions, should be developed and improved. ARGs
in bioaerosols are mainly detected by culture-based methods such
as Kirby Bauer disk diffusion and qPCR, which can not completely
cover full diversity of microorganisms and ARGs in airborne
bioaerosols (King et al., 2020). High-throughput sequencing
shows great potential due to its consideration of full diversity
(Veillette et al., 2018). However, the lack of research on ARGs in
bioaerosols makes the advantages, disadvantages and applicable
conditions of various detection methods still unclear. According
to the characteristics of bioaerosols and sampling sites, selecting
appropriate sampling and detection methods of ARGs, using
methods in conjunction with other methods or developing new
technologies need further study, which may make the detection
results more reliable and facilitate risk assessment and model
exposure.
(2) The technology of controlling bioaerosols at present is mainly to
reduce bioaerosols by inactivating microorganisms and some
limitations of them hinder their up-scaled applications. For
example, plasma technology produces charged ionized gaseous
materials with high energy by ionizing gas to inactivate micro­
organisms quickly. However, they wear equipment and consume
a lot of energy. Microwave technology, using electromagnetic
wave radiation to inactivate microorganisms also has these dis­
advantages (Wang et al., 2019b). Photocatalysis disinfection
technology, which can destroy cell membranes of bacteria and
even their RNA and DNA through generating free electrons and
electron holes with high oxidation, seems to show high applica­
tion prospects due to high inactivation efficiency and few sec­
ondary pollution (Hu et al., 2020b). However, whether these
bioaerosols removal technologies can stably and efficiently
remove ARGs in biolaerosols still remain to be further explored
due to the lack of research.
(3) For ARG risk assessment in bioaerosols, the mature system has
not been established, making the harm of ARGs to human beings
ambiguous. Although some studies have made qualitative or
quantitative assessment of the risk of ARGs, these assessment
systems have some limitations. The existing quantitative risk
assessments of ARGs either lack appropriate parameters, dose-
response relationships or exposure probability (Cyprowski
et al., 2019). Qualitative risk assessments also lack dose-response
relationships. Additionally, they may lack consideration of ARG
release in natural environment or gene mutation (Martínez et al.,
2015), which needs further research. The risk assessment of ARGs
in bioaerosols is a complex and comprehensive project. As
mentioned in this paper, it involves many interrelated factors.
Therefore, close cooperation and joint efforts of scientific re­
searchers in many fields may be needed to solve this problem in
the future.
11
Journal of Cleaner Production 348 (2022) 131094
6.2. Outlooks
ARGs in water or soil can enter the atmosphere by aerosolization,
resulting in a wider propagation range than in water or soil. Hence, the
control of ARG pollution in the air is inseparable from the control of
ARGs in water and soil. However, most researchers only focus on the
generation and transmission of ARGs in bioaerosols at present, and do
not connect them with ARGs in soil and water (Gwenzi et al., 2021). On
the issue of regional and even global ARGs management, the atmo­
sphere, water and soil should be regarded as a whole, especially the
ARGs in bioaerosols, so as to minimize ARG contamination. Addition­
ally, ARGs in bioaerosols are closely related to nature and human beings.
As mentioned in Section 2 and 5, the propagation of airborne ARGs is
affected by human activities and natural conditions such as weather and
terrain. Therefore, these factors should be considered when studying the
spread of ARGs in bioaerosols and its response measures.
Developing the technology of removing ARGs in bioaerosols and
reducing the emission of ARGs from the source is very important to
control airborne ARG pollution. The current technology is only limited
to the inactivation of microorganisms in bioaerosols and it is unclear
whether the ARGs they carry can continue to spread. Hence, improving
the existing technologies and developing new technologies that can
effectively remove ARGs and MGEs in bioaerosols to control the trans­
mission of ARGs in the air is very necessary. Additionally, reducing the
generation of ARGs from the source is also very important for controlling
airborne ARG pollution, such as reducing the use of antibiotics and
improving relevant treatment processes (e.g., reducing the release of
bioaerosols through covering the composting facilities with biofilm a
semi-permeable membrane and combined process of sewage treatment
and bioaerosol inactivation) (Cui et al., 2020).
Due to the wide spread of ARGs, which leads to a wide range of
transmission, the control of airborne ARG pollution may require the
joint consultation and cooperation of countries worldwide. For example,
the government should take measures to formulate appropriate rules or
relevant laws to limit the use of antibiotics and reduce the transmission
of ARGs through limiting the import of meat food, tourism. Additionally,
the operation standardization (e.g., timely ventilation and use of per­
sonal protective equipment) in workplaces with high ARG exposure
concentration in the air such as landfill sites should be strengthened. If
necessary, emissions trading can also be considered for the emission of
biolaerosols with ARGs.
7. Conclusions
In this article, the production, dissemination, harm, and composite
pollution of bioaerosols carrying ARGs and the factors affecting trans­
mission were discussed. Although ARGs in bioaerosols come from a wide
range of sources and can be widely spread with the help of natural
conditions such as wind and wave, airborne ARG contamination seems
to have not attracted enough attention, which is reflected by few rele­
vant studies. Additionally, the complicated environmental factors,
including meteorological, climate change, seasonal, geographic condi­
tions, location and epidemic virus factors, affect the transmission of
ARGs in bioaerosols, which makes it very difficult to control ARG
pollution in the air. Especially, the compound pollution of ARGs in
bioaerosols needs further research to control the transmission of them
and alleviate airborne ARG pollution effectively. Notably, there are
more sources of airborne ARG emissions than mentioned in this article,
for example, farmland, gardens, and any place where ARGs may occur.
Similarly, pollutants that form compound pollution with ARGs in the air
and the factors affecting their generation and transmission are also
highly complex and thus require further research. To reduce the gen­
eration of ARGs, reducing the use of antibiotics fundamentally is
necessary, which is conductive to reducing the selection pressure on
microorganisms and requires intergovernmental cooperation to formu­
late relevant regulations or laws. Additionally, improving risk
P. Chen et al. Journal of Cleaner Production 348 (2022) 131094

assessment, developing efficient technologies of detecting and removing Cui, P., Bai, Y., Li, X., Peng, Z., Chen, D., Wu, Z., Zhang, P., Tan, Z., Huang, K., Chen, Z.,
Liao, H., Zhou, S., 2020. Enhanced removal of antibiotic resistance genes and mobile
ARGs in bioaerosols requires in-depth research to control ARG pollution
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Environ. 660, 288–296. https://doi.org/10.1016/j.scitotenv.2018.12.356.
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