Evaluation of micro-well collector for capture and analysis of aerosolized Bacillus subtilis spores
Evaluation of micro-well collector for capture and analysis of aerosolized Bacillus subtilis spores
Jiayang He 0 1
Nicola K. Beck 1
Alexandra L. Kossik 1
Jiawei Zhang 0 1
Edmund Seto 1
John Scott Meschke 1
Igor Novosselov 0 1
0 University of Washington, Mechanical Engineering , Seattle, WA , United States of America, 2 University of Washington, Department of Environmental and Occupational Health Sciences , Seattle, WA , United States of America
1 Editor: Ryan Kelly, Pacific Northwest National Laboratory , UNITED STATES
Bioaerosol sampling and identification are vital for the assessment and control of airborne pathogens, allergens, and toxins. In-situ analysis of chemical and biological particulate matter can significantly reduce the costs associated with sample preservation, transport, and analysis. The analysis of conventional filters is challenging, due to dilute samples in large collection regions. A low-cost cartridge for collection and analysis of aerosols is developed for use in epidemiological studies and personal exposure assessments. The cartridge collects aerosol samples in a micro-well which reduces particles losses due to the bounce and does not require any coating. The confined particle collection area (dwell~1.4 mm) allows reducing the elution volume for subsequent analysis. The performance of the cartridge is validated in laboratory studies using aerosolized bacterial spores (Bacillus subtilis). Colony forming unit analysis is used for bacterial spore enumeration. Cartridge collection efficiency is evaluated by comparison with the reference filters and found to be consistent with tested flow rates. Sample recovery for the pipette elution is ~80%. Due to the high density of the collected sample, the cartridge is compatible with in-situ spectroscopic analysis and sample elution into the 10±20 μl liquid volume providing a significant increase in sample concentration for subsequent analysis.
Data Availability Statement: All relevant data will
be within the paper and its Supporting Information
Funding: This research was partially funded by a
grant from the National Institute of Environmental
Health Sciences (grant numbers 1R21ES024715
and 1R33ES024715 to Edmund Seto); and by a
grant from the National Institute of Biomedical
Imaging and Bioengineering (grant number U01
EB021923 to Edmund Seto). The funders had no
role in study design, data collection and analysis,
Many environmental and occupational exposure studies are aimed at understanding negative
effects of bioaerosols on human health. Exposure to bioaerosols is of interest in occupational
settings like dairy farms, textile plants, and grain processing and the indoor air studies, e.g. [1±
6]. Traditionally aerosol particles are collected onto a solid substrate or filter media, into a
liquid volume, or directly deposited onto a growth media. Several techniques have been used for
the collection of bioaerosols, including filter collection, centrifugal collection, electrostatic
precipitation, liquid impingement, and impaction. Often, filters are used for aerosol sample
collection; multiple publications describe these collection and elution procedures, review the
decision to publish, or preparation of the
Competing interests: The authors have declared
that no competing interests exist.
collection efficiency of a variety of filtration media for submicron inert and biological particles.
Recent reviews include performance and comparison of multiple samplers related to the
collection of bioaerosols [7±10]. With respect to direct personal exposure monitoring some of
these methods may not be practical; for example, filter collection and analysis is limited by
high elution volumes, the form factor of the sampling setup, and high-power requirements.
Due to the development in miniaturization of sampling pumps and electronics, new exposure
methods are becoming more popular in epidemiological studies and air quality monitoring
applications. Recent examples of miniature PM samplers are presented in [11±14] including
biological aerosol collectors [15±19], real-time time PM monitoring devices [20±23], and
lowcost distributed sensor networks [24±26] that are used for pollution exposure estimates.
Solid substrate collectors, such as cyclone and inertial impactors, rely on the momentum
difference between airborne particulates and air molecules to collect the aerosol particles onto
a solid surface. Commercially available surface collectors have been widely used by the
researchers, for example, Andersen impactor directly collects the organisms onto a growth
media; it has been used for the collection of many biological agents, including molds, fungal
spores, and bacterial spores, e.g., [
]. However, a limitation of this method is the potential
to overload the collection substrate, which occurs when multiple organisms impact at the same
location. Liquid collection methods originally suffered from liquid evaporation, particle
bounce, and liquid loss due to aerosolization and vaporization, e.g., AGI-30 impingers [
]. The BioSampler (SKC Inc., Eighty-Four, PA) was developed to increase the sampling
duration and improve the collection efficiency of viable organisms. Collection through
impaction and centrifugal motion allows for the particles to be collected in non-evaporating, more
viscous liquids, increasing the sampling time and maintaining relatively constant physical
collection efficiencies [
]. Most devices based on sampling and collection into liquid volume
require significant power due to their high air flow rate; their large liquid volume sample limits
their applicability in personal samplers and analysis techniques where small collection volume
and direct integration with microfluidic devices is desired. Recently, several air-to-liquid
interfaces for microfluidic devices have been reported [
19, 32, 33
]. For atmospheric science and
security applications where concentrations of aerosols can be relatively low, additional particle
concentrations may be required. Virtual impactors [
] and aerodynamic lens concentrators
can increase the concentration by order of magnitude with minimum pressure drop while
reducing the size of the particle beam [
Primarily two types of the samplers are used to assess exposure and to characterize the
environment of interest: (i) area and (ii) personal exposure samplers. Typically, area samplers are
operated at high flow rates, greater than 10 standard liters per minute (slpm). For
epidemiological studies, personal samplers are preferred as they allow to assess the individual exposure
removing the ambiguity of temporal and spatial distribution of particulate matter.
Miniaturization and integration of components for personal exposure monitors require the
development and validation of novel aerosol collectors; it also presents an opportunity to improve
analysis methods and enable rapid in-situ sample characterization. Recently, we presented a
design methodology for a combined an aerodynamic focusing (AF) inlet and a μ-well trap
compatible with a small sample elution volume and in-situ optical analysis [
techniques such as UV laser-induced fluorescence (UV-LIF) and Raman spectroscopy have
been used for classification and quantitative determination of the aerosol particles [38±42].
Spectra obtained from a cluster of aerosol particles collected on the substrate provide the
information about chemical compositions and biological identification of the particles. The
cartridge presented in this work is designed using the previously described methodology and has
been manufactured using high-volume fabrication method for application in the
epidemiological research. To enable in-situ UV based analysis, the cartridge is fabricated using UV
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transparent materials. The dimensions of the inlet (which act as an elution port) and the
micro-well (μ-well) are optimized for compatibility with the standard pipette tip and
high-volume fabrication methods.
In this work, we present the performance of the low-cost μ-well aerosol collection cartridge
designed for use with the personal exposure monitor. The performance of the cartridge is
validated in laboratory studies using aerosolized single-organism, Bacillus subtilis spores based on
comparison with the collection and analysis of the reference filters. Sample recovery for the
pipette elution is tested for elution in the 10±20 μl liquid volume.
Micro-well cartridge design and fabrication
The design of the low-cost μ-well collection cartridge is based on the methodology outlined in
our previous work [
]. The low-cost collection cartridge presented here consists of two
injection-molded parts (see Fig 1). The top half includes an AF inlet to accelerate and focus the
particles and a fluidic connection to the vacuum pump. The conical μ-well on the bottom half
captures the particles into a small collection area. The range of the operating flow rate for the
cartridge is 0.75±2 slpm at standard conditions (293 K, 101 kPa). The principle of operation
has been previously described, typical flow field and particle behavior are shown in Figs A-B in
S1 File. The Stokes number analysis is used to estimate the performance of the AF inlet, is used
as the guidance of the inlet design. If the particle Stokes number of the AF inlet is smaller than
the optimum Stokes number, the particles follow the flow streamlines cannot be effectively
focused into the well. In contrast, if the Stokes number is near the optimum value, the particle
is focused by the AF inlet and projected into the μ-well. The optimum Stokes number Stk was
selected to be 1, based on the previous studies [
] and our own work based on the CFD
simulations of a number of focusing inlet geometries and flow rates . Stk ~ 0.55±0.85 have
been reported for aerodynamic focusing using parallel slit geometries [
]. The optimizing
parameter is used as the design guidance; it does not account for variation of the Stoke number
Fig 1. (a) The photograph of the assembled μ-well aerosol collection cartridge and (b) the cartridge in a disassembled state.
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in a non-uniform velocity field, in reality, the Stokes number may vary significantly depending
on the particle position, its size and density, and the device flow rate. Stk is calculated as:
where Cc is the Cunningham slip correction factor for the particle, ρp is the particle density, dp
is the particle diameter, U is the area-averaged flow axial velocity magnitude at a well upstream
location, η is the gas viscosity, and Dc is the characteristic dimension, which, in this case, is the
diameter of the nozzle.
The geometry of the inlet also satisfies the practical considerations of the compatibility with
a standard pipette tip for the sample elution. The diameter of the inlet is chosen based on the
calculation of the Stokes number, as well as compatibility with the standard pipette tip. The
angle of the μ-well cone of 35 degrees is selected to reduce the effect of particle bounce at the
collection location. Our previous study shows that larger angles are more effective for the
mitigation of particle bounce; however, they are less efficient for the collection of smaller particles.
Fig 1A shows the photograph of the cartridge with arrows indicating the flow direction. Fig 1B
shows the cartridge in a disassembled state to reveal the μ-well on the bottom half of the
cartridge. The design drawings are shown in Fig C in S1 File.
The μ-well cartridges are fabricated using the injection molding technique. The cost of each
cartridge is under $5 for low production run (n = 500) with the aluminum mold used. Each
collector is assembled from two molded parts, with a gasket between them. A 0.5 mm thick
silicone gasket is used to provide the proper nozzle-to-plate distance; the gasket thickness can be
changed to vary the distance between the nozzle and the μ-well, which, in turn, changes the
cartridge collection characteristics. The seal between the nozzle and the impaction plate is
achieved by applying compression force from the two snap-on tabs. All collectors are checked
for a vacuum seal before conducting the experiments. The dimensions of a collector are about
40 mm × 23 mm × 5 mm. Other critical dimensions of the AF inlet and the μ-well are shown
in Fig C in S1 File. Both the inlet and outlet of the μ-well cartridge are located on the same side
of the geometry to permit the easy integration of the collector array and the vacuum manifold,
as well as to ensure proper sealing to avoid sample contamination during storage and
handling. The overall quality of the injection-molded μ-well cartridge was found to be very good:
the production parts did not have the defects often associated with injection molding, such as
sinking, burning, flashing, or short shots. All tested collector assemblies fit together well and
provided a good seal for all tested operating pressures. The pressure drop through the
collectors was found to be consistent for any given flow rate within the accuracy of the measuring
The collection efficiency of the cartridge was evaluated by collecting aerosolized
single-organisms B. subtilis (ATCC1 31578™ Strain Designation: RUB331) in comparison with the
collection of the reference filters. The collection experiments were performed in a custom 0.3 m3
stainless steel, well mixed aerosol chamber (see Fig 2) for a range of flow rates of 0.75±2.0
slpm. The large volume of the chamber with mixing fans provides well-mixed conditions and
allows for evaluation multiple collectors simultaneously. The aerosol concentration in the
chamber was found to be spatially uniformed with the operation of the mixing fans. Typically
an array of six collectors and three reference filters were used in the experiments. The
collectors are fluidically connected to the mass flowmeters (HONEYWELL, Morristown, NJ,
AWM5102VN) via an adapter. The reference filter housed in the filter housing, similarly
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Fig 2. The configuration of the aerosol chamber experiment.
connected house vacuum through the same type flow meters. Three reference filters (Spectrum
Poretics1 polycarbonate membrane filters, 47mm, 0.6 μm pore sizes) in open face aerosol
filter holders (EDM Millipore, Billerica, MA, model XX5004710) collect particles at 1 slpm in
each experiment. All flowmeters are located outside the chamber allowing for individual
control of the flow rate during the experiment. The flowmeters are calibrated before and after each
experiment using Gillibrator (Sensidyne, Clearwater, FL, Gilibrator 2). All experiments were
performed at the room temperature of 20±25ÊC and relative humidity in the chamber of 40±
60%. Operating flow rates for the cartridges were 0.75, 1, 1.5, and 2 slpm.
A B. subtilis spore stock was prepared by initially growing the B. subtilis overnight in
LuriaBertani Broth (LB) at 37Ê C in an incubator shaker. The overnight culture was spread on AK#2
sporulating agar, and the plates were incubated for 48 hours at 37Ê C. The growth was scraped
off the plates, and the stock was stored in water at 4Ê C. The stock was purified by centrifuging
at 10,000 G for 10 minutes and washed in cold, sterile water; this procedure was repeated three
times. Subsequently, the pellet was shaken overnight at 125 rpm and 4Ê C, centrifuged for 20
minutes at 20,000 g and resuspended in the new cold, sterile water. This procedure was
repeated for several days until the pellet formed a homogeneous layer. The stock was checked
for purity with microscopy using a malachite green spore stain. The purified stock was stored
at 4Ê C.
The prepared bacterial spore suspension was diluted 100x in the distilled water right before
the experiment. During the experiment, 4 mL of prepared solution was nebulized from the
liquid suspension with 20 psi clean air using a Lovelace nebulizer (In-Tox Products, Moriarty,
NM). An aerodynamic particle sizer (APS 3321, TSI, Shoreview, MN) was used to verify the
particle size and monitor the particle concentration in the chamber. The aerodynamic
diameter of the B. subtilis spores was measured by the APS to be about 0.75 μm. APS measurements
also confirm that no significant particle agglomeration occurs inside the chamber during the
experiment. Fig 3 shows a typical particle size distribution during the experiments.
Following the collection experiment, two elution steps were performed to remove B. subtilis
from the collectors. The efficiency of each elution procedure was quantified. The first elution
step is used quantify the sample collected in the in μ-well and in the close vicinity (1-2mm)
around the well. The second step is used to elute all the particulate matter collected elsewhere
inside the cartridge during the experiment; these include the particles lost on the upper
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Fig 3. The size distribution of airborne particles.
collector part, the gasket, and around the outlet of the cartridge. For the first elution, small
liquid aliquots were used: 2 x 10 μl of Phosphate Buffered Saline (PBS) with 0.05% Tween 20.
Each 10 μl was added to the collector and immediately pipetted up/down 10 times, after which
the droplet was placed in a microcentrifuge tube containing 980 μl of PBS and vortexed for 1
minute before diluting in PBS. A second elution consists of disassembling and submerging the
entire cartridge in a centrifuge tube with 10 ml of PBS with 0.05% Tween. The centrifuge tube
undergoes 10 minutes of shaking on a shaker table, followed by 5 minutes of sonication in a 60
Fig 4. The measured pressure drop of the collection cartridge at different flow rates.
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Watts ultrasonic cleaner bath (model #gb928). After the collection, the reference filters were
submerged in 10 ml of PBS with 0.05% Tween and underwent a 10-min shaking period,
followed by 5 minutes of sonication. While sonication is a recognized method of spore recovery
], experiments plating dilutions of the B. subtilis spore stock show that the sonication
step may reduce the spore stock titer by up to 30%.
The elution efficiency and the collection efficiency were calculated by comparing the B.
subtilis Colony forming unit (CFU) for the cartridge and the reference filter elution, the flow rate
adjustments were made to account for differences in sampling rates. The collection efficiencies
are calculated based on the results of at least 6 data points from three runs for each flow
condition. Mean, and one σ error bars are presented in the collection efficiency plot. CFU was
quantified on nutrient agar plates by plating 100 μl of the relevant dilutions in duplicate and
incubating at 37Ê C overnight, after which the CFU captured at each flow rate were
enumerated. The undiluted sample and a 10x dilution were plated for the first elution of the cartridge;
the undiluted samples were plated for the second elution. Both the undiluted and the 10x
dilution were plated for the reference filters. In the analysis, the CFU counts were adjusted for the
difference in elution volumes between the first, the most concentrated eluent, the reference
filters, and the second elution step.
Results and discussion
To estimate the power consumption and to aid with the selection of the pump for the personal
exposure monitors, we evaluated the cartridge for pressure drop as a function of the flow rates.
Fig 4 shows the measured pressure drop for the cartridge, as well as the pressure drop
predicted by the computational fluid dynamics (CFD). The pressure drop was measured using a
Magnehelic gauge (Series 2100 Magnehelic1 Differential Pressure Gage, Dwyer, Michigan
City, IN). Three measurements are performed for each operating condition; the measurement
error did not exceed 5%. The pressure drop in the cartridge was mostly due to the losses in the
nozzle and the abrupt change of the flow direction at the impaction plate. The experimental
pressure drop of the low-cost cartridge was compared to the results of the computational fluid
dynamics study performed during the design stage [
]. The results show excellent agreement
between the computational and experimental pressure drop measurements. The cartridges are
evaluated for potential failure due to the collection overloading. The pressure drop of an
overloaded cartridge was consistent with the blank one; this indicates that loading of the collector
does not increase the pressure drop, unlike filter collection [
Bioaerosol collection efficiencies and analysis
The collection efficiencies are presented in Fig 5. The results show that the collection efficiency
for the B. subtilis spore increases with the flow rate. At a flow rate of 0.75 slpm, the cartridge
collects about 35% of the B. subtilis spores as compared to the number collected by the
reference filter. The maximum collection efficiency observed is about 80% at the highest flow rate
tested (2 slpm). The results are consistent with the inertial mechanism of particle capture. The
particle with the lower Stokes number, associated with the low velocities in the focusing inlet,
can not reach the μ-well wall [
]. Higher sampling rates are desired to improve the capture
efficiency of single-organism bioaerosols. Unlike conventional impactors without coating, no
significant collection efficiency drop associated with particle bounce is observed in the
collection of B. subtilis as the majority of the spores were recovered from the direct well elution
(elution 1); less than 25% was recovered during the second elution when the cartridge was
disassembled and sonicated. The limited particle loss from the targeted collection area can be
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Fig 5. B. subtilis collection efficiencies in μ-well inertial impactors as a function of the collector flow rate.
attributed to the μ-well angle, which redirects the bounce toward the bottom of the well and
greatly eliminates the particles from re-entering the major flow. Though the preliminary
results from the chamber experiments and the pilot indoor and outdoor sampling show
significant accumulation of sample in the μ-well (see Fig D in S1 File), the bounce mechanisms for
biological and other particles needs further investigation. A single pipette elution extracts
more than 75% of the B. subtilis collected in the μ-well cartridge for all tested conditions. The
small elution volume is beneficial for bioaerosol sampling providing two to three order
magnitude preconcentration of the analysis volume. We tested the cartridge compatibility with the
fluorescence measurement using the fluorescent PSL microspheres. The method and the setup
used for the measurement is described in the SI document. The spectrum from the in-situ
fluorescence measurement on the cartridge shows a good agreement with the spectrum acquired
from the liquid sample (see Fig E in S1 File).
Conclusions and discussions
Performance of a low-cost μ-well aerosol cartridge is evaluated for collection and analysis of
single-organism B. subtilis spores. The design of the device is based on practical considerations
for sample analysis; the inlet dimensions are compatible with the pipette sample elution and
integration with personal exposure monitors. The cartridge collects highly concentrated
particle samples in a 1 mm diameter spot. The sample is retained in the well because the particle
bounce is redirected toward the center of the well, increasing the sample collection density.
Collection efficiency is consistent for each flow condition. Sample recovery for the pipette
elution is greater than 75%. The elution volume used to recover the collected sample from the
cartridge is in the range of 10±20 μl, which provides a high preconcentration of the aerosol
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sample for liquid assays, based on the cartridge geometry the volume can be further reduced if
the procedure is automated or microfluidic analysis is desired.
While in this manuscript we use the standard laboratory analysis method, the optically
transparent collection substrate and well-defined collection region allow for the in-situ optical
analysis of the collected aerosols. This in-situ spectroscopic analysis may provide a
nondestructive orthogonal data such as fluorescent measurement and a significant reduction in
analysis cost for monitoring exposure to chemical and biological aerosols, toxic compounds in
indoor environment and other applications. In our preliminary analysis (see Supplemental
Materials), we demonstrated the in-situ detection of fluorescent 2 μm PSL spheres collected in
the aerosol chamber experiments. The optimization of the optical cell geometry is required to
minimize the scatter and reflection from the cartridge surfaces. One promising approach is to
use fiber-optic excitation and collection of the signal in a backscatter probe configuration; this
would significantly minimize the sensor footprint. Multiple reviews in the topic of bio and
chemical detection using fiber-optic sensor exist, e.g., [
]. Raman backscatter probes are
well-developed, e.g., [51±53] and can be readily used with the cartridge without significant
hardware modification. Fiber-optic probes for surface-enhanced Raman  and anti-stokes
] have been demonstrated for analysis for detection of bioaerosols. Sample collected
in the μ-well can be an analysis based on native fluorescence of the bioaerosols such as UV LIF
], though the application of this technique using fiber-optic bundles needs further
S1 File. Fig A. Gas streamlines; The colormap represents the air velocity magnitude in m/s
(Nozzle diameter: 0.8 mm; Re = 1815).
Fig B. Trajectories of particles in different impactors at 1 slpm. (a) particle trajectories in the
AF μ-well impactor. The dashed area is expanded in (b) to show the details; (c) detailed view of
the particle trajectories for the μ-well impactor with a straight nozzle. Particle size: red line±
3 μm, green line± 2 μm, blue line± 1 μm (Nozzle Diameter: 0.8mm; Re = 1815).
Fig C. (a) The μ-well aerosol collection cartridge and (b) the dimensions of the cartridge; (c)
the critical dimensions of the AF inlet and the μ-well (unit: mm).
Fig D. Microscopic image of PM collected in the cartridges during the one-week usability
Fig E. (a) The cartridge fluorescence measurement setup and (b) the fluorescent PSL particle
collection site; (c) the fluorescence spectrum for the liquid and solid sample.
This research was partially funded by a grant from the National Institute of Environmental
Health Sciences (grant numbers 1R21ES024715 and 1R33ES024715); and by a grant from the
National Institute of Biomedical Imaging and Bioengineering (grant number U01 EB021923).
Data curation: Jiayang He, Nicola K. Beck, Alexandra L. Kossik, Jiawei Zhang.
Formal analysis: Jiayang He, Nicola K. Beck.
Funding acquisition: Edmund Seto.
Investigation: Jiayang He, Edmund Seto.
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Methodology: John Scott Meschke, Igor Novosselov.
Supervision: John Scott Meschke, Igor Novosselov.
Validation: John Scott Meschke.
Writing ± original draft: Jiayang He, Nicola K. Beck.
Writing ± review & editing: Jiayang He, Edmund Seto, Igor Novosselov.
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