Environment International 118 (2018) 189–193
Contents lists available at ScienceDirect
Environment International
journal homepage: www.elsevier.com/locate/envint
A review on recent progress in observations, and health effects of
bioaerosols
T
Charmi Humbala, Sneha Gautama, , Ujwalkumar Trivedib
⁎
a
b
Department of Environmental Science and Engineering, Marwadi University, Rajkot 360003, India
Department of Microbiology, Faculty of Science, Marwadi University, Rajkot 360003, India
A R T I C LE I N FO
A B S T R A C T
Keywords:
Bioaerosol
Health effects
Respiratory diseases
Cancer
Bioaerosol is a particulate mixture of solid and semi-solid matter combined with biotic matter like pollens,
microbes and their fragments. The present review stresses on a cumulative understanding of sources, components, quantification and distribution of bioaerosols with respect to size, and its significant impacts on human
health. The present review will be instrumental in devising strategies to understand and manage bioaerosols and
reducing their human exposure and associated health hazards. The present review aims explore the relationship
between particle and associated biological agents responsible for behaviours like dispersal, total potential health
hazards and toxicology level during exposure to bioaerosol.
1. Introduction
Previous (Mandal and Brandl, 2011; Chen and Hildemann, 2009)
indicated generation of bioaerosol due to human activities (i.e.,
sneezing/coughing, washing floors/toilet cleaning, walking/talking
etc.). Dedesko et al. (2015) demonstrated the influence of meteorological parameters (i.e., temperature, and humidity) on formation and
dispersion of bioaerosols. Moreover, Srikanth et al. (2008) suggested
the relationship between bioaerosols and human diseases such as influenza, lungs diseases, allergies etc. The immunomodulatory or immunostimulatory effects of bioaerosols contribute significantly in the
development of adaptive immunity. However, the over exposure can
cause hyperactive stimulation of immune system causing allergic responses (Severson et al., 2010). A number of bioaerosol studies assesses
the impact of bioaerosols on living organisms, but the exact role and
mechanism of pathogenesis remain illusive. Fig. 1 highlights different
types of microorganisms associated with bioaerosols and associated
diseases.
A comprehensive review has been presented through reviewed approximately published article in English language journals only that
reported bioaerosols, source and its impact on human health. The
findings from computer searches by using of some keywords (i.e.,
bioaerosols, diseases, exposure, and health problems), will help to
readers for better understanding on impact of bioaerosols on human
health.
Bioaerosols are a particulate mixture of dust, microbes and their
fragments. They are transmitted through air with a particle size ranging
from 0.001 nm to 100 μm. The pathophysiological effects of these
bioaerosol pollutants depend on their size, concentration, physiochemical properties and size distribution (Mandal and Brandl, 2011).
Because of the micro to nano scale size, bioaerosol scan easily deposit in
various parts of the body via lungs, and circulatory system. Such deposition can cause a number of health complications involving single
organ to an entire organ system (Georgakopoulos et al., 2009). These
are alarming reasons why awareness of bioaerosols is of great importance and hence it becomes necessary to investigate the source
distributions and their impacts on human health.
Massive industrial development and population expansion has
caused deleterious anthropogenic activities (waste sorting and composting, agricultural, the livestock industry and food processing activities) (Ghosh et al., 2015). Exposure of human to bioaerosols in populated countries like China, India etc. is a primary concern because of
associated adverse health impacts (Pearson et al., 2015). Many recent
studies revealed that enhancement in the level of bioaerosols has become a serious environmental concern (Ghosh et al., 2015; Lacey and
Dutkiewicz, 1994). Not only humans but pet and husbandry animals are
also distressed from increasing prevalence of the bioaerosol exposer. In
recent decades, bioaerosols are reported to contribute as much as up to
34% indoor air pollution with life threatening consequences (Mandal
and Brandl, 2011).
⁎
Corresponding author.
E-mail address: sneha.gautam@marwadieducation.edu.in (S. Gautam).
https://doi.org/10.1016/j.envint.2018.05.053
Received 17 April 2018; Received in revised form 28 May 2018; Accepted 31 May 2018
0160-4120/ © 2018 Published by Elsevier Ltd.
2. Sampling methods
Size and composition of airborne bioaerosol depend on their
Environment International 118 (2018) 189–193
C. Humbal et al.
Species
Diseases
Infections
Species
Diseases
Legionella
pheumophila
Legionnaires
Inhalation of aerosol with
containing bacteria
Mycobacterium
tuberculosis
Varibrio cholera
Cholera
Taking contaminated water/air
Typhoid
Taking contaminated water
Bacillus anthracis
spore
Anthrax
Salmonella Typhi
Varibrio cholerae
Cholera
Morbillivirus measles
Mumps & Rubella Coughing / sneezing; bodily fluids
Bordetella pertussis
Whooping Cough
Tuberculosis
InfecƟons
Inhalation of contaminated air
Taking contaminated water/air
Taking contaminated water/air
Inhalation of contaminated air
2 – 3 µm
< 1 – 2 µm
Size
Fig. 1. Microbes in bioaerosols and their related diseases.
Hänninen, 2006), and yeast extract glucose chloramphenicol (YGC)
(Borrego et al., 2012). Fibrous filter made of a fine fibrous mat, where
the particle is captured while passing the filter is also very efficient.
Similarly, few filters have a pore-like structure in which particles are
deposited (Uhrbrand et al., 2011). However, it can be seen that the
efficiency is affected by several factors such as measurement time, relative humidity, temperature, microbial species (Wang et al., 2001).
Moreover, glass – impinger method was found to be very suitable
method to collect bacteria and fungi from the air streams (Thorne et al.,
1992). Li (1999) compared to using impinger to collect bioaerosol and
filtration methods.
formation and mechanical stress in particular environmental conditions. Therefore, the selection of sampling tool to monitor the concentration level of bioaerosol should be quite different from the general
employed procedure for analysis. Very few research articles could be
found on new sampling methods to assess the bioaerosol and its microbial analysis. However, previous employed methods such as impingers, cyclones, impactors, filters, spore traps, electrostatic precipitation, thermal precipitators, condensation traps, gravitational
samplers, etc. of common particle are being used to collect the
bioaerosol with or without modification (Haig et al., 2016). Moreover,
many samplers have been reported to separate the particle from the air
through gravity (Wang et al., 2001), centrifugal force (Haig et al.,
2016) and other methods (i.e., Filtration, Electrostatic Precipitator
Thermal Precipitator etc.) (Ghosh et al., 2015). According to particle
size, few options are available such as inertial bioaerosol sampler (i.e.,
sieves, stacked sieves, and impactors), which rely on properties of the
particle to deviate from laden gas flow due to inertia (Haig et al., 2016).
Moreover, non-inertial bioaerosol samplers (i.e., filtration, electrostatic
precipitator, and thermal precipitator) are also available to show nondependency (i.e., less reliant on particle size) upon the selective particle
size (Ghosh et al., 2015).
Impingers and cyclones method are being used to collect airborne
particle in the liquid medium. In case of impinge, it is operated through
the gas flow from the inlet to collection chamber containing liquid,
where number of factors (i.e., gas flow rate, distance from inlet to
outlet, and surface of the liquid) are influenced by the size and diameter
of the particle (Han and Mainelis, 2012). On the other hand, centrifugal
force worked in cyclone (conventional), where air is forced into the
collection chamber by the vortex formed in the system. Macher et al.
(1995) reported that new cyclone sampling techniques to collect the
sample through standard centrifuge tube from the top of the sampler
chamber instead of the peripheral portion of the system. Such an optimization makes procedure very simple (Macher et al., 1995). Moreover, the investigators also reported high efficiency with multiple tubes
to identify size fractioned samples (i.e. large, medium and small – sized
bioaerosols) in initial (centrifuge) tube, second tube, and filter, respectively.
Media plays a vital role in the collection of bioaerosol. The most
commonly used is a filter to transfer bioaerosol on a plate or in liquid
for further analysis (i.e., microscopic examination or culturing experiments) (Wu et al., 2010). Several studies are reported stating utilization
of different forms of cultivation media like maltextractagar (MEA)
(Lehtinen et al., 2013), Sabouraud dextrose agar (SDA) (Park et al.,
2015), dichloran rose-bengal chloramphenicol (DRBC) (Tolvanen and
3. Components of bioaerosols
Bioaerosols pose a substantial health risk globally (Burger, 1990;
Kim et al., 2017). Bioaerosols comprise of diverse classes of microorganisms and their products. The major microbial constituents are
fungi and bacteria while their products constitute endotoxin, mycotoxins, and allergens (Kim et al., 2017). A recent focus is also stretched
upon the presence of Beta-glucans (a common cell-wall component of
fungi) in bioaerosol which causes a number of health-related consequences such as cancer, auto-immune diseases and severe respiratory
tract dysfunctions. Looking at the severity of bioaerosol in health
management, it is, therefore, essential to understand the nature and
components of bioaerosols. This section discusses the classification of
major microbial (and their products) constituents of bioaerosols.
3.1. Fungi
Fungi are ubiquitously present in nature over a wide range of environmental condition (Lee et al., 2006). The kingdom fungi consist of a
diverse group of eukaryotic organism ranging from microscopic to
macroscopic in size. A recent survey estimates about 2.2 million to
3.8 million species of fungus existing in almost all the terras of the earth
(Hawksworth and Lücking, 2017). The pathogenic fungal species like
Aspergillus spp., Fusarium spp., Scedosporium spp., and Mucorales spp.
are most common components in bioaerosol (Diaz-Guerra et al., 2000;
Grigis et al., 2000; Jung et al., 2009). These fungi are known to cause a
number of health-related related complications such as acute toxicity,
hypersensitivity (majorly asthma), invasive mycoses and respiratory
abnormalities (Bush and Portnoy, 2001; Jung et al., 2009; Verhoeff and
Burge, 1997).
Near all the known species of fungi possess the ability to propagate
(in air or water as a particulate) via sporulation. The fungal spores can
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4.1. Respiratory effects
survive in a wide range of physio-chemical conditions making them a
persistent bioaerosol (Górny et al., 2001).
Respiration is of the major gateway of bioaerosol in human lungs.
Respiratory exposure of bioaerosol associated to allergens, pollens, and
microbes causes a number of respiratory diseases. Maheswaran et al.
(2014) reported respiratory exposure on 422 Canadian children's,
where 7–10 years and 11–14 years of children affected by non-atopic/
non-atopic asthma (OR = 1.79, 95%, CI: 4941.14–2.81) and bronchial
hyper-responsiveness (OR = 4951.74, 95% CI: 1.05–2.89), respectively. Moreover, Ma et al. (2015) suggested positively higher asthma
intensity with mold sensitivity. Asthma with mold sensitivity in children's bedrooms (OR = 4.82, 95%, CI: 1.29–18.02) and living rooms
(OR = 7.5195%, CI: 1.49–37.8) reported by Karvonen et al. (2015). In
other hand, Baldacci et al. (2015) observed that exposure to pollen is
responsible for decreased lung function and a significant increase in the
pulmonary inflammation. Similarly, 15% asthma epidemic are reported
due to presence of grass pollen (Canova et al., 2013). Hoppin et al.
(2014) reported that irritating airways and inflammation are caused
due to presence of endotoxin and glucans from bacteria and molds.
Lung function decreases significantly upon exposure to endotoxins
(80 mg and 20 mg for health subject and asthmatics subjects, respectively) (Kharitonov and Sjöbring, 2007).
3.2. Bacteria
Bacteria constitute a very large domain of prokaryotic microorganisms which are found to dwell in almost all the terra of the earth
including the extreme environment (extremophiles) (Van den Burg,
2003). It is estimated that about 107 to 109 species of bacteria are
present on earth of which only 10,000 are known due to their stringent
growth requirements (Curtis et al., 2002; Schloss and Handelsman,
2004). Bacteria are very diverse in terms of the metabolism and morphology with the size ranging from 0.3 μm (Mycoplasma) to 0.5 mm
(Thiomargarita namibiensis) (Robertson et al., 1975; Schulz and
Jorgensen, 2001; Williams, 2011). Air is known to be a salient carrier of
a number of airborne pathogenic bacteria like Bordetella pertussis, Bacillus anthracis, Corynebacterium diphtheriae and Neisseria meningitidis
which are known to be causative organisms of Pertusis, Anthrax,
Diphtheriae and Meningitis, respectively (GBD 2013 Mortality and
Causes of Death Collaborators, 2015; Heininger, 2010; Hendricks et al.,
2014; Theilen et al., 2008). These organisms can deliver a lethal effect
to human upon transmission as bioaerosol. Many Bacillus species
transmitted as bioaerosol are known to be potent allergens causing
respiratory tract discomfort (Fierer et al., 2008).
4.2. Communicable diseases
3.3. Endotoxins
Transmission of pathogenic microbes via bioaerosol carriers are the
responsible for the communicable disease via direct contact (i.e.,
licking, touching, etc.) or indirect contact (i.e., cough and sneeze)
(Chretien et al., 2015; Baker and Gray, 2009; Vanrompay et al., 2007).
Wu et al. (2015) reported the number of cases of zoonotic infections on
farmer or workers which are directly or indirectly associated with veterinary practices, livestock farms and catching animals. These infected
subjects work as medium to communicate the diseases from one person
to another one through family get-together, society programs and associated animals they pet. Ling et al. (2015) reported the higher distribution of bacteria Chlamydophilapsittaci through birds especially pigeons and psittacine birds. Commandeur et al. (2014) conducted study
to identify the high infection of microorganism on worker, those associated with goat farms in Netherland over three years survey. And
found a large number of patients (approximately 4000) were visited
and reported at MHS (municipal health services) in same time period
(Roest et al., 2011). Table 1 shows comprehensive summary of communicable diseases due to higher level of biological agent.
The lipopolysaccharide component of Gram-negative bacterial cell
wall is known as an endotoxin which further consists of a lipid component –Lipid A that displays the toxic effect to the host (Armstrong
et al., 2013; Kim et al., 2017; Tirsoaga et al., 2007). Endotoxins are
mainly released upon the cellular and can bind to the dust particles
causing its respiratory exposure (Duquenne et al., 2013; MattsbyBaltzer et al., 1991). Routine occupational exposure of endotoxin contaminated bioaerosols are known to cause an array of occupational
hazards like hypersensitivity, septic shock, fever, chest congestion,
systemic inflammatory response, respiratory system dysfunction and
even death (Park et al., 2015; Thilsing et al., 2015). In severe cases,
human exposure to such bioaerosols also caused lung cancer
(Hayleeyesus et al., 2015; Johnson and Choi, 2012).
3.4. β glucans
β glucans are the cell wall component of fungi made up of glucose
polymers where glucose moiety can be linked through β(1 → 3), β(1 →
4) and β(1 → 6) glycosidic bonds (Manzi and Pizzoferrato, 2000). Although, β glucans are routinely used to treat diabetes and elevated
blood cholesterol, harmful effects of over exposure to β glucans contaminated bioaerosols vary from immunomodulatory responses to allergic reactions (Kim et al., 2017; Manzi and Pizzoferrato, 2000).
4.3. Cancer
Several studies suggest a significant correlation between cancer
subjects and exposure to bioaerosol (Hayleeyesus et al., 2015; Hoppin
et al., 2014; Johnson and Choi, 2012). Review study done by Johnson
and Choi (2012) demonstrated the involvement of meat and poultry
related industries responsible for lung cancer.
They also suggested that contribution of bioaerosol including
dander, feather, skin material, and microbes are more prominent than
smoking in meat/poultry industry causing 30% excess risk of lung
cancer due to bioaerosol. On the other hand, Mclean et al. (2004) reported the significant contribution of higher exposure to bioaerosol
including animal urine, virus, faecal matter etc., on workers and associates in meat/poultry area by utilizing the dose–response relationship. Felini et al. (2011) reported the higher exposure to bioaerosol due
to industrial (meat/poultry) activities such as gathering of live chickens
(OR = 3.6, 95% CI: 1.2–10.9), meat distribution center (OR = 8.9, 95%
CI: 2.7–29.3), and other activities (OR = 4.8, 95% CI: 1.5–16.6). Similarly, earlier studies pointed out on pancreatic cancer due to higher
exposure (OR = 3.0, 95% CI:1.0–8.2) to bioaerosol in associated
worker of pig farm (Johnson and Choi, 2012; Felini et al., 2011). Several researchers identified high risk of lung cancer through the
4. Health exposure to bioaerosols
Bioaerosol distribution in the atmosphere adversely affects human
health via various mechanisms (Van Leuken et al., 2016; Pearson et al.,
2015). The pathophysiology of bioaerosols depends on their physical,
biological and chemical properties (Pearson et al., 2015; Yoon et al.,
2011). However, the composition of bioaerosols is very complex and
assessment of their comprehensive toxicity is difficult (Pearson et al.,
2015). Toxicity of an individual component may not be sufficient to
understand its overall toxicity (Thorne, 2000, 2001). The toxicity can
vary depending on a number of factors such as oxidative potential, and
its microbial composition. Therefore, chemical characterization is essential. The characterization is likely to vary with source types, i.e., a
particular source type may be associated with a typical chemical signature of the bioaerosol (Thorne, 2001).
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Table 1
Comprehensive details of recent results/observations of communicable diseases through biological agent.
Study location (s)
Biological agent
Key observations
Authors (year)
Netherlands
Australia
Italy
–
Animals shed C. burnetii
influenza A (H7N7) virus
Bacteria
USA
Bacteria
Denmark
Bacteria
Taking control measures during collection goat/vaccinations, and the culling of pregnant infected
animals.
Exposed population to become infected (infd50) was 1.5 bacteria (95% confidence interval:
0.75–38.7).
Observed in higher concentration in milk, urine, faeces and birth products.
High level of exposure identified in poultry farms.
Introduced to new area such as potential protective effects of microbial exposures on atopy and
atopic diseases, and other potential health effects such as skin and neurological conditions and birth
effects.
Genetic studies suggested strategies for treatment and vaccine development to minimize the impacts
due to biological agents.
Observed the significant impact of biological agent during inhalation, where Mycobacterium
tuberculosis (Mtb) contaminated air or presence of bacteria enters in deeper part of lungs.
To identified high exposure to communicable diseases in teachers, children and health care workers.
Dijkstra et al. (2012)
Netherlands
Culling of pregnant
infected animals.
Coxiella burnetii
Bacteria, virus
Brooke et al. (2013)
Parker et al. (2006)
Puzelli et al. (2014)
Douwes et al. (2003)
Berrington and Hawn
(2013)
Pedersen et al. (2016)
Rohani and Drake (2011)
Acknowledgements
relationship between higher exposure and industrial activities
(slaughtering/collecting/distribution of chickens) (Felini et al., 2012;
McLean et al., 2004). Furthermore, recent study reported by Gandhi
et al. (2014) found the comprehensive details about the high risk of
brain cancer in 46,819 workers associated with poultry/non-poultry
industrial area, where slaughtering (OR = 5.8, 95% CI: 1.2–28.3) and
working in of shell–fish farm (OR = 13.0, 95% CI: 1.9–84.2).
We are thankful to Marwadi University, Rajkot, Gujarat, India for
providing the financial support and manpower to carry out field study
and research. We acknowledge valuable suggestions and critical insights provided by the faculties of Department of Environmental
Science and Engineering and Department of Microbiology, Marwadi
University Rajkot.
5. Future perspectives and conclusions
References
A number of possible directions and key research challenges on
prediction and control of bioaerosol can be identified. These may include:
Bioaerosol measurement and monitoring: All applied monitoring
methods should be precise and must be according to standard guidelines, to collect accurate data with minimum loss/error. Moreover,
methods should contain all possible factors i.e., specific location and
climatic condition to assess accurate quantitative and qualitative observations and relevant data, to make specific policies.
Biological, microbiological and chemical analysis: The detection
of microorganisms, organic and inorganic components in bioaerosol is
essential for the identification of toxicological properties of bioaerosol
and its possible impact on the human health. Tempo-spatial methods
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