Access to this full-text is provided by Springer Nature.
Content available from Scientific Reports
This content is subject to copyright. Terms and conditions apply.
1
Scientific RePoRtS | (2018) 8:2752 | DOI:10.1038/s41598-018-21058-w
www.nature.com/scientificreports
Far-UVC light: A new tool to control
the spread of airborne-mediated
microbial diseases
David Welch, Manuela Buonanno, Veljko Grilj, Igor Shuryak, Connor Crickmore,
Alan W. Bigelow, Gerhard Randers-Pehrson, Gary W. Johnson & David J. Brenner
Airborne-mediated microbial diseases such as inuenza and tuberculosis represent major public
health challenges. A direct approach to prevent airborne transmission is inactivation of airborne
pathogens, and the airborne antimicrobial potential of UVC ultraviolet light has long been established;
however, its widespread use in public settings is limited because conventional UVC light sources are
both carcinogenic and cataractogenic. By contrast, we have previously shown that far-UVC light
(207–222 nm) eciently inactivates bacteria without harm to exposed mammalian skin. This is because,
due to its strong absorbance in biological materials, far-UVC light cannot penetrate even the outer
(non living) layers of human skin or eye; however, because bacteria and viruses are of micrometer or
smaller dimensions, far-UVC can penetrate and inactivate them. We show for the rst time that far-UVC
eciently inactivates airborne aerosolized viruses, with a very low dose of 2 mJ/cm2 of 222-nm light
inactivating >95% of aerosolized H1N1 inuenza virus. Continuous very low dose-rate far-UVC light
in indoor public locations is a promising, safe and inexpensive tool to reduce the spread of airborne-
mediated microbial diseases.
Airborne-mediated microbial diseases represent one of the major challenges to worldwide public health1.
Common examples are influenza2, appearing in seasonal3 and pandemic4 forms, and bacterially-based
airborne-mediated diseases such as tuberculosis5, increasingly emerging in multi-drug resistant form.
A direct approach to prevent the transmission of airborne-mediated disease is inactivation of the correspond-
ing airborne pathogens, and in fact the airborne antimicrobial ecacy of ultraviolet (UV) light has long been
established6–8. Germicidal UV light can also eciently inactivate both drug-sensitive and multi-drug-resistant
bacteria9, as well as diering strains of viruses10. However, the widespread use of germicidal ultraviolet light in
public settings has been very limited because conventional UVC light sources are a human health hazard, being
both carcinogenic and cataractogenic11,12.
By contrast, we have earlier shown that far-UVC light generated by ltered excimer lamps emitting in the 207
to 222 nm wavelength range, eciently inactivates drug-resistant bacteria, without apparent harm to exposed
mammalian skin13–15. e biophysical reason is that, due to its strong absorbance in biological materials, far-UVC
light does not have sucient range to penetrate through even the outer layer (stratum corneum) on the surface of
human skin, nor the outer tear layer on the outer surface of the eye, neither of which contain living cells; however,
because bacteria and viruses are typically of micron or smaller dimensions, far-UVC light can still eciently
traverse and inactivate them13–15.
e earlier studies on the germicidal ecacy of far UVC light13,15–18 were performed exposing bacteria irradi-
ated on a surface or in suspension. In that a major pathway for the spread of inuenza A is aerosol transmission3,
we investigate for the rst time the ecacy of far-UVC 222-nm light for inactivating airborne viruses carried by
aerosols – with the goal of providing a potentially safe alternative to conventional 254-nm germicidal lamps to
inactivate airborne microbes.
Results
Virus inactivation. Figure1 shows representative uorescent 40× images of mammalian epithelial cells
incubated with airborne viruses that had been exposed in aerosolized form to far-UVC doses (0, 0.8, 1.3 or 2.0
mJ/cm2) generated by ltered 222-nm excimer lamps. Blue uorescence was used to identify the total number of
Center for Radiological Research, Columbia University Medical Center, New York, New York, 10032, USA.
Correspondence and requests for materials should be addressed to D.W. (email: dw2600@cumc.columbia.edu)
Received: 7 November 2017
Accepted: 29 January 2018
Published: xx xx xxxx
OPEN
There are amendments to this paper
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
2
Scientific RePoRtS | (2018) 8:2752 | DOI:10.1038/s41598-018-21058-w
cells in a particular eld of view, while green uorescence indicated the integration of live inuenza A (H1N1)
viruses into the cells. Results from the zero-dose control studies (Fig.1, top le) conrmed that the aerosol
irradiation chamber eciently transmitted the aerosolized viruses through the system, aer which the live virus
eciently infected the test mammalian epithelial cells.
Figure2 shows the surviving fraction, as a function of the incident 222-nm far-UVC dose, of exposed H1N1
aerosolized viruses, as measured by the number of focus forming units in incubated epithelial cells relative to
unexposed controls. Linear regressions (see below) showed that the survival results were consistent with a classi-
cal exponential UV disinfection model with rate constant k = 1.8 cm2/mJ (95% condence intervals 1.5–2.1 cm2/
mJ). e overall model t was good, with a coecient of determination, R2 = 0.95, which suggests that most of the
Figure 1. Antiviral ecacy of dierent low doses of 222-nm far-UVC light. Typical uorescent images of
MDCK epithelial cells infected with inuenza A virus (H1N1). e viruses were exposed in aerosolized form
in the irradiation chamber to doses of 0, 0.8, 1.3 or 2.0 mJ/cm2 of 222-nm far-UVC light. Infected cells uoresce
green (blue = nuclear stain DAPI; green = Alexa Fluor-488 conjugated to anti-inuenza A antibody). Images
were acquired with a 40× objective.
Figure 2. Quantication of the antiviral ecacy of 222-nm far-UVC light. Fractional survival, FFUUV/
FFUcontrols, is plotted as a function of the 222-nm far-UVC dose. Means and standard deviations refer to
triplicate repeat studies and the line represents the best-t regression to Eqn1 (see text).
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
3
Scientific RePoRtS | (2018) 8:2752 | DOI:10.1038/s41598-018-21058-w
variability in virus survival was explained by the exponential model. e rate constant of 1.8 cm2/mJ corresponds
to an inactivation cross-section (dose required to inactivate 95% of the exposed viruses) of D95 = 1.6 mJ/cm2 (95%
condence intervals 1.4–1.9 mJ/cm2).
Discussion
We have developed an approach to UV-based sterilization using single-wavelength far-UVC light generated by l-
tered excilamps, which selectively inactivate microorganisms, but does not produce biological damage to exposed
mammalian cells and tissues13–15. e approach is based on biophysical principles in that far-UVC light can trav-
erse and therefore inactivate bacteria and viruses which are typically micrometer dimensions or smaller, whereas
due to its strong absorbance in biological materials, far-UVC light cannot penetrate even the outer dead-cell
layers of human skin, nor the outer tear layer on the surface of the eye.
Here we applied this approach to test the ecacy of the 222-nm far-UVC light to inactivate inuenza A virus
(H1N1) carried by aerosols in a benchtop aerosol UV irradiation chamber, which generated aerosol droplets of
sizes similar to those generated by human coughing and breathing. Aerosolized viruses owing through the irra-
diation chamber were exposed to UVC emitting lamps placed in front of the chamber window.
As shown in Fig.2, inactivation of inuenza A virus (H1N1) by 222-nm far-UVC light follows a typical
exponential disinfection model, with an inactivation cross-section of D95 = 1.6 mJ/cm2 (95% CI: 1.4–1.9). For
comparison, using a similar experimental arrangement, but using a conventional 254 nm germicidal UVC lamp,
McDevitt et al.19 found a D95 value of 1.1 mJ/cm2 (95% CI: 1.0–1.2) for H1N1 virus. us as we13,15 and others16–18
reported in earlier studies for bacterial inactivation, 222-nm far-UVC light and 254-nm broad-spectrum germi-
cidal light are also comparable in their eciencies for aerosolized viral inactivation. Other recent work compar-
ing viral inactivation across the UVC spectrum has shown variations in eciency are expected, but in general
both regions of the spectrum are eective in inactivation, though the precise cause of inactivation may dier20,21.
However as discussed above, based on biophysical considerations and in contrast to the known human health
safety issues associated with conventional germicidal 254-nm broad-spectrum UVC light, far-UVC light does not
appear to be cytotoxic to exposed human cells and tissues in vitro or in vivo13–15.
If these results are conrmed in other scenarios, it follows that the use of overhead low-level far-UVC light
in public locations may represent a safe and ecient methodology for limiting the transmission and spread of
airborne-mediated microbial diseases such as inuenza and tuberculosis. In fact the potential use of ultraviolet
light for airborne disinfection is by no means new, and was rst demonstrated more than 80 years ago8,22. As
applied more recently, airborne ultraviolet germicidal irradiation (UVGI) utilizes conventional germicidal UVC
light in the upper part of the room, with louvers to prevent direct exposure of potentially occupied room areas23.
is results in blocking more than 95% of the UV radiation exiting the UVGI xture, with substantial decrease
in eectiveness24. By contrast, use of low-level far-UVC xtures, which are potentially safe for human exposure,
could provide the desired antimicrobial benets without the accompanying human health concerns of conven-
tional germicidal lamp UVGI.
A key advantage of the UVC based approach, which is in clear contrast to vaccination approaches, is that
UVC light is likely to be eective against all airborne microbes. For example, while there will almost certainly
be variations in UVC inactivation eciency as dierent inuenza strains appear, they are unlikely to be large7,10.
Likewise, as multi-drug-resistant variants of bacteria emerge, their UVC inactivation eciencies are also unlikely
to change greatly9.
In conclusion, we have shown for the rst time that very low doses of far-UVC light eciently inactivate
airborne viruses carried by aerosols. For example, a very low dose of 2 mJ/cm2 of 222-nm light inactivates >95%
of airborne H1N1 virus. Our results indicate that far-UVC light is a powerful and inexpensive approach for pre-
vention and reduction of airborne viral infections without the human health hazards inherent with conventional
germicidal UVC lamps. If these results are conrmed in other scenarios, it follows that the use of overhead very
low level far-UVC light in public locations may represent a safe and ecient methodology for limiting the trans-
mission and spread of airborne-mediated microbial diseases. Public locations such as hospitals, doctors’ oces,
schools, airports and airplanes might be considered here. is approach may help limit seasonal inuenza epi-
demics, transmission of tuberculosis, as well as major pandemics.
Methods
Far-UVC lamps. We used a bank of three excimer lamps containing a Kr-Cl gas mixture that predomi-
nantly emits at 222 nm25,26. e exit window of each lamp was covered with a custom bandpass lter designed to
remove all but the dominant emission wavelength as previously described15. Each bandpass lter (Omega Optical,
Brattleboro, VT) had a center wavelength of 222 nm and a full width at half maximum (FWHM) of 25 nm and
enables >20% transmission at 222 nm. A UV spectrometer (SPM-002-BT64, Photon Control, BC, Canada) with
a sensitivity range between 190 nm and 400 nm was utilized to verify the 222 nm emission spectrum. A deute-
rium lamp standard with a NIST-traceable spectral irradiance (Newport Model 63945, Irvine, CA) was used to
radiometrically calibrate the UV spectrometer. An SM-70 Ozone Monitor (Aeroqual, Avondale, Auckland, New
Zealand) measured the ozone generation from the lamps to be <0.005 ppm, which is not a signicant level to
provide an antimicrobial eect to aerosolized viruses27.
Far-UVC dosimetry. Optical power measurements were performed using an 818-UV/DB low-power UV
enhanced silicon photodetector with an 843-R optical power meter (Newport, Irvine, CA). Additional dosimetry
to determine the uniformity of the UV exposure was performed using far-UVC sensitive lm as described in our
previous work28,29. is lm has a high spatial resolution with the ability to resolve features to at least 25 µm, and
exhibits a nearly ideal cosine response30,31. Measurements were taken between experiments therefore allowing
placement of sensors inside the chamber.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
4
Scientific RePoRtS | (2018) 8:2752 | DOI:10.1038/s41598-018-21058-w
A range of far-UVC exposures, from 3.6 µJ/cm2 up to 281.6 mJ/cm2, were used to dene a response calibration
curve. Films were scanned as 48 bit RGB TIFF images at 150 dpi using an Epson Perfection V700 Photo atbed
scanner (Epson, Japan) and analyzed with radiochromic lm analysis soware32 to calculate the total exposure
based on measured changes in optical density.
Measurements using both a silicon detector and UV sensitive lms were combined to compute the total dose
received by a particle traversing the exposure window. e three vertically stacked lamps produced a nearly
uniform dose distribution along the vertical axis thus every particle passing horizontally through the irradiation
chamber received an identical dose. e lamp width (100 mm) was smaller than the width of the irradiation
chamber window (260 mm) so the lamp power was higher near the center of the irradiation chamber window
compared to the edge. e UV sensitive lm indicated a power of approximately 120 µW/cm2 in the center third
of the window and 70 µW/cm2 for the outer thirds. e silicon detector was used to quantify the reectivity of
the aluminum sheet at approximately 15% of the incident power. Combining this data allowed the calculation of
the average total dose of 2.0 mJ/cm2 to a particle traversing the window in 20 seconds. Additionally, the silicon
detector was used to conrm the attenuation of 222-nm light through a single sheet of plastic lm was 65%. e
addition of one or two sheets of plastic lm between the lamps and the irradiation chamber window yielded aver-
age doses of 1.3 mJ/cm2 and 0.8 mJ/cm2, respectively.
Benchtop aerosol irradiation chamber. A one-pass, dynamic aerosol / virus irradiation chamber was
constructed in a similar conguration to that used by Ko et al.33, Lai et al.34, and McDevitt et al.19,35. A schematic
overview of the system is shown in Fig.3 and is pictured in Fig.4. Aerosolized viruses were generated by adding
a virus solution into a high-output extended aerosol respiratory therapy (HEART) nebulizer (Westmed, Tucson,
AZ) and operated using a dual-head pump (ermo Fisher 420–2901–00FK, Waltham, MA) with an input
ow rate of 11 L/min. e aerosolized virus owed into the irradiation chamber where it was mixed with inde-
pendently controlled inputs of humidied and dried air. Humidied air was produced by bubbling air through
water, while dry air was provided by passing air through a desiccant air dryer (X06–02–00, Wilkerson Corp,
Richland, MI). Adjusting the ratio of humid and dry air enabled control of the relative humidity (RH) within the
irradiation chamber which, along with the nebulizer settings, determined the aerosol particle size distribution.
An optimal RH value of 55% resulted in a distribution of aerosol particle sizes similar to the natural distribution
from human coughing and breathing, which has been shown to be distributed around approximately 1 µm, with
a signicant tail of particles less than 1 µm36–38.
Aer combining the humidity control inputs with the aerosolized virus, input ow was directed through
a series of baes that promoted droplet drying and mixing to produce an even particle distribution and sta-
ble humidity34. The RH and temperature inside the irradiation chamber were monitored using an Omega
RH32 meter (Omega Engineering Inc., Stamford, CT) immediately following the baes. A Hal Technologies
HAL-HPC300 particle sizer (Fontana, CA) was adjoined to the irradiation chamber to allow for sampling of
particle sizes throughout operation.
During UV exposure, the 222-nm lamps were placed 11 cm from the irradiation chamber window. e lamps
were directed at the 26 cm × 25.6 cm chamber window which was constructed of 254-µm thick UV transparent
plastic lm (Topas 8007x10, Topas Advanced Polymers, Florence, KY), and which had a transmission of ~65% at
222 nm. e wall of the irradiation chamber opposite the transparent window was constructed with polished alu-
minum in order to reect a portion of the UVC light back through the exposure region, therefore increasing the
overall exposure dose by having photons pass in both directions. e depth of the irradiation chamber between
the window and the aluminum panel was 6.3 cm, creating a total exposure volume of 4.2 L.
Figure 3. Schematic diagram of the custom UV irradiation chamber. e chamber is depicted in a top down
view. Components of the setup include: water bubbler for humidied air input (A), a desiccator for dry air input
(B), a nebulizer (C), baes (D), an RH and temperature meter (E), a particle sizer (F), far-UVC lamps (G), band
pass lters (H), a far-UVC transmitting plastic window (I), a reective aluminum surface (J), and a BioSampler
(K). Pumps are used to pressurize the nebulizer for aerosol generation and to control ow through the system.
Flow control valves allow adjustments through the system. HEPA lters are included on all air inputs and
outputs. A set of three way valves controls ow to or around the BioSampler. e vertically stacked lamps are
directed at the window in the side of the chamber to expose the aerosols passing horizontally. e additional
lms to uniformly decrease the dose were placed between the lters and the window. e path of the aerosolized
virus within the system during sampling is indicated with the red dotted line.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
5
Scientific RePoRtS | (2018) 8:2752 | DOI:10.1038/s41598-018-21058-w
Flow of the aerosols continues out of the irradiation chamber to a set of three way valves that could be cong-
ured to either pass through a bypass channel (used when no sampling was required), or a BioSampler (SKC Inc,
Eighty Four, PA) used to collect the virus. e BioSampler uses sonic ow impingement upon a liquid surface to
collect aerosols when operated at an air ow of 12.5 L/min. Finally, ow continued out of the system through a
nal HEPA lter and to a vacuum pump (WP6111560, EMD Millipore, Billerica, MA). e vacuum pump at the
end of the system powered ow through the irradiation chamber. e ow rate through the system was governed
by the BioSampler. Given the ow rate and the total exposure volume of the irradiation chamber, 4.2 L, a single
aerosol droplet passed through the exposure volume in approximately 20 seconds.
e entire irradiation chamber was set up inside a certied class II type A2 biosafety cabinet (Labconco,
Kansas City, MO). All air inputs and outputs were equipped with HEPA lters (GE Healthcare Bio-Sciences,
Pittsburgh, PA) to prevent unwanted contamination from entering the chamber as well as to block any of the virus
from releasing into the environment.
Irradiation chamber performance. e custom irradiation chamber simulated the transmission of aero-
solized viruses produced via human coughing and breathing. e chamber operated at a relative humidity of 55%
which resulted in a particle size distribution of 87% between 0.3 µm and 0.5 µm, 11% between 0.5 µm and 0.7 µm,
and 2% > 0.7 µm. A comparison to published ranges of particle size distributions is shown in Table1. Aerosolized
viruses were eciently transmitted through the system as evidenced from the control (zero exposure) showing
clear virus integration (Fig.1, top le).
Experimental protocol. e virus solution in the nebulizer consisted of 1 ml of Dulbecco’s Modied Eagle’s
Medium (DMEM, Life Technologies, Grand Island, NY) containing 108 focus forming units per ml (FFU/ml) of
inuenza A virus [A/PR/8/34 (H1N1)], 20 ml of deionized water, and 0.05 ml of Hank’s Balanced Salt Solution
with calcium and magnesium (HBSS++). e irradiation chamber was operated with aerosolized virus particles
owing through the chamber and the bypass channel for 15 minutes prior to sampling, in order to establish
the desired RH value of ~55%. Sample collection initiated by changing air ow from the bypass channel to the
BioSampler using the set of three way valves. e BioSampler was initially lled with 20 ml of HBSS++ to capture
the aerosol. During each sampling time, which lasted for 30 minutes, the inside of the irradiation chamber was
Figure 4. Photograph of the custom UV irradiation chamber. e experimental setup shows many of the
necessary components while some elements, such as pumps, lters, and lamps, were omitted to better depict the
overall setup.
Particle Size Distribution
<1.0 µm>1.0 µm
Papineni 199740 Coughing 83–91% 9–16%
Mouth Breathing 83–95% 4–16%
Nose Breathing 83–100% 0–16%
Talking 77–88% 11–22%
0.3–0.5 µm 0.5–0.7 µm>0.7 µm
is work 87% 11% 2%
Table 1. Example particle size distributions from humans during various activities are given along with the
measured values for this work.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
6
Scientific RePoRtS | (2018) 8:2752 | DOI:10.1038/s41598-018-21058-w
exposed to 222 nm far-UVC light through the UVC semi-transparent plastic window. Variation of the far-UVC
dose delivered to aerosol particles was achieved by inserting additional UVC semi-transparent plastic lms, iden-
tical to the material used as the chamber window, between the lamps and the chamber window. e extra plastic
lms uniformly reduced the power entering the chamber. e three test doses of 0.8, 1.3 and 2.0 mJ/cm2, were
achieved by adding two, one, or no additional plastic lms, respectively. Zero-dose control studies were con-
ducted with the excimer lamps turned o. Experiments at each dose were repeated in triplicate. A newly sterilized
BioSampler was used for each experimental run to prevent unwanted contamination. Negative controls, where
virus was omitted from the nebulizer mixture, were run intermittently and showed no virus collection in the
BioSampler. Aer the sampling period was completed the solution from the BioSampler was used for the virus
infectivity assay.
Virus infectivity assay. We measured viral infectivity with a focus forming assay that employs standard u-
orescent immunostaining techniques to detect infected host cells and infectious virus particles39. Briey, aer run-
ning through the irradiation chamber for 30 minutes, 0.5 ml of virus suspension collected from the BioSampler
was overlaid on a monolayer of Madin-Darby Canine Kidney (MDCK) epithelial cells routinely grown in DMEM
supplemented with 10% Fetal Bovine Serum (FBS), 2 mM L-alanyl-L-glutamine, 100 U/ml penicillin and 100 μg/
ml streptomycin (Sigma-Aldrich Corp. St. Louis, MO, USA). Cells were incubated with the virus for 45 minutes,
washed three times with HBSS++ and incubated overnight in DMEM. Infected cells were then xed in 100% ice
cold methanol at 4 °C for 5 minutes and labeled with inuenza A virus nucleoprotein antibody [C43] (Abcam
ab128193, Cambridge, MA) 1:200 in HBSS++ containing 1% bovine serum albumin (BSA; Sigma-Aldrich Corp.
St. Louis, MO, USA) at room temperature for 30 minutes with gentle shaking. Cells were washed three times
in HBSS++ and labeled with goat anti-mouse Alexa Fluor-488 (Life Technologies, Grand Island, NY) 1:800 in
HBSS++ containing 1% BSA at room temperature for 30 minutes with gentle shaking. Following three washes
in HBSS++, the cells were stained with Vectashield containing DAPI (4′,6-diamidino-2-phenylindole) (Victor
Laboratories, Burlingame, CA) and observed with the 10× and 40× objectives of an Olympus IX70 uorescent
microscope equipped with a Photometrics PVCAM high-resolution, high-eciency digital camera. For each
sample, at least three elds of view of merged DAPI and Alexa-488 images were acquired. Image-Pro Plus 6.0
soware (Media Cybernetics, Bethesda, MD) was used to analyze the 10× images to measure the FFUUV as the
ratio of cells infected with the virus divided by the total number of cells.
Data analysis. e surviving fraction (S) of the virus was calculated by dividing the fraction of cells that
yielded positive virus growth at each UV dose (FFUUV) by the fraction at zero dose (FFUcontrols): S = FFUUV/
FFUcontrols. Survival values were calculated for each repeat experiment and natural log (ln) transformed to bring
the error distribution closer to normal40. Linear regression was performed using these normalized ln[S] values
as the dependent variable and UV dose (D, mJ/cm2) as the independent variable. Using this approach, the virus
survival (S) was tted to rst-order kinetics according to the equation7:
=− ×kDln[S], (1)
where k is the UV inactivation rate constant or susceptibility factor (cm2/mJ). e regression was performed
with the intercept term set to zero, which represents the denition of 100% relative survival at zero UV dose.
Bootstrap 95% condence intervals for the parameter k were calculated using R 3.2.3 soware41. e virus inac-
tivation cross section, D95, which is the UV dose that inactivates 95% of the exposed virus, was calculated as
D95 = −ln[1 − 0.95]/k.
References
1. Global, regional, and national life expectancy, all-cause mortality, and cause-specic mortality for 249 causes of death, 1980–2015:
a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388, 1459–1544 (2016).
2. Paules, C. & Subbarao, . Inuenza. Lancet 390, 697–708 (2017).
3. Cowling, B. J. et al. Aerosol transmission is an important mode of inuenza A virus spread. Nat Commun 4, 1935 (2013).
4. Yu, I. T. et al. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N Engl J Med 350, 1731–1739 (2004).
5. Pai, M. et al. Tuberculosis. Nat ev Dis Primers 2, 16076 (2016).
6. Hollaender, A., du Buy, H. G., Ingraham, H. S. & Wheeler, S. M. Control of air-borne microorganisms by ultraviolet oor irradiation.
Science 99, 130–131 (1944).
7. owalsi, W. J. Ultraviolet Germicidal Irradiation Handboo: UVGI for Air and Surface Disinfection, (New Yor: Springer).
8. Wells, W. F. & Fair, G. M. Viability of B. Coli Exposed to Ultra-Violet adiation in Air. Science 82, 280–281 (1935).
9. Conner-err, T. A., Sullivan, P. ., Gaillard, J., Franlin, M. E. & Jones, . M. e eects of ultraviolet radiation on antibiotic-
resistant bacteria in vitro. Ostomy Wound Manage 44, 50–56 (1998).
10. Budowsy, E. I., Bresler, S. E., Friedman, E. A. & Zheleznova, N. V. Principles of selective inactivation of viral genome. I. UV-induced
inactivation of inuenza virus. Arch Virol 68, 239–247 (1981).
11. Setlow, . B., Grist, E., ompson, . & Woodhead, A. D. Wavelengths eective in induction of malignant melanoma. Proc Natl Acad
Sci USA 90, 6666–6670 (1993).
12. Balasubramanian, D. Ultraviolet radiation and cataract. J Ocul Pharmacol er 16, 285–297 (2000).
13. Buonanno, M. et al . 207-nm UV light - a promising tool for safe low-cost reduction of surgical site infections. I: in v itro studies. PLoS
One 8, e76968 (2013).
14. Buonanno, M. et al. 207-nm UV Light-A Promising Tool for Safe Low-Cost eduction of Surgical Site Infections. II: In-Vivo Safety
Studies. PLoS One 11, e0138418 (2016).
15. Buonanno, M. et al. Germicidal Ecacy and Mammalian Sin Safety of 222-nm UV Light. adiat. es. 187, 483–491 (2017).
16. Matafonova, G. G., Batoev, V. B., Astahova, S. A., Gómez, M. & Christo, N. Eciency of rCl excilamp (222 nm) for inactivation
of bacteria in suspension. Lett. Appl. Microbiol. 47, 508–513 (2008).
17. Sosnin, E. A., Avdeev, S. M., uznetzova, E. A. & Lavrent’eva, L. V. A Bactericidal Barrier-Discharge rBr Excilamp. Instruments and
Experimental Techniques 48, 663–666 (2005).
18. Wang, D., Oppenländer, T., El-Din, M. G. & Bolton, J. . Comparison of the Disinfection Eects of Vacuum-UV (VUV) and UV
Light on Bacillus subtilis Spores in Aqueous Suspensions at 172, 222 and 254 nm. Photochem and Photobiol 86, 176–181 (2010).
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
7
Scientific RePoRtS | (2018) 8:2752 | DOI:10.1038/s41598-018-21058-w
19. McDevitt, J. J., udnic, S. N. & adonovich, L. J. Aerosol Susceptibility of Inuenza Virus to UV-C Light. Appl. Environ. Microbiol.
78, 1666–1669 (2012).
20. Bec, S. E., Hull, N. M., Poepping, C. & Linden, . G. Wavelength-Dependent Damage to Adenoviral Proteins Across the Germicid al
UV Spectrum. Environ. Sci. Technol. (2017).
21. Bec, S. E. et al. Comparison of UV-Induced Inactivation and NA Damage in MS2 Phage across the Germicidal UV Spectrum.
Appl. Environ. Microbiol. 82, 1468–1474 (2016).
22. eed, N. G. e history of ultraviolet germicidal irradiation for air disinfection. Public Health ep 125, 15–27 (2010).
23. Nardell, E., Vincent, . & Sliney, D. H. Upper-room ultraviolet germicidal irradiation (UVGI) for air disinfection: a symposium in
print. Photochem Photobiol 89, 764–769 (2013).
24. udnic, S. N. et al. Spatial distribution of uence rate from upper-room ultraviolet germicidal irradiation: Experimental validation
of a computer-aided design tool. HVAC& esearch 18, 774–794 (2012).
25. ahmani, B., Bhosle, S. & Zissis, G. Dielectric-Barrier-Discharge Excilamp in Mixtures of rypton and Molecular Chlorine. IEEE
Trans Plasma Sci 37, 546–550 (2009).
26. Sosnin, E. A., Avdeev, S. M., Taraseno, V. F., Saun, V. S. & Schitz, D. V. rCl barrier-discharge excilamps: Energy characteristics
and applications. Instrum Exp Tech 58, 309–318 (2015).
27. eez, M. M. & Sattar, S. A. A new ozone-based method for virus inactivation: preliminary study. Phys. Med. Biol. 42, 2027 (1997).
28. Welch, D., anders-Pehrson, G., Spotnitz, H. M. & Brenner, D. J. Unlaminated Gafchromic EBT3 Film for Ultraviolet adiation
Monitoring. adiat. Prot. Dosim. 176, 341–346 (2017).
29. Welch, D., Spotnitz, H. M. & Brenner, D. J. Measurement of UV Emission from a Diusing Optical Fiber Using adiochromic Film.
Photochem and Photobiol 93, 1509–1512 (2017).
30. Drobny, J. G. Dosimetry and adiometry. In adiation Technology for Polymers, Second Edition 215–231 (CC Press, 2010).
31. rins, A., Bolsée, D., Dörschel, B., Gillotay, D. & nusche, P. Angular Dependence of the Eciency of the UV Sensor Polysulphone
Film. adiat. Prot. Dosim. 87, 261–266 (2000).
32. Mendez, I., Peterlin, P., Hudej, ., Strojni, A. & Casar, B. On multichannel lm dosimetry with channel-independent perturbations.
Med Phys 41, 011705 (2014).
33. o, G., First, M. W. & Burge, H. A. Inuence of relative humidity on particle size and UV sensitivity of Serratia marcescens and
Mycobacterium bovis BCG aerosols. Tubercle and Lung Disease 80, 217–228 (2000).
34. Lai, . M., Burge, H. A. & First, M. W. Size and UV Germicidal Irradiation Susceptibility of Serratia marcescens when Aerosolized
from Dierent Suspending Media. Appl. Environ. Microbiol. 70, 2021–2027 (2004).
35. McDevitt, J. J. et al. Characterization of UVC Light Sensitivity of Vaccinia Virus. Appl. Environ. Microbiol. 73, 5760–5766 (2007).
36. Chao, C. Y. H. et al. Characterization of expiration air jets and droplet size distributions immediately at the mouth opening. J.
Aerosol Sci 40, 122–133 (2009).
37. Papineni, . S. & osenthal, F. S. e Size Distribution of Droplets in the Exhaled Breath of Healthy Human Subjects. J. Aerosol Med
10, 105–116 (1997).
38. Morawsa, L. et al. Size distribution and sites of origin of droplets expelled from the human respiratory tract during expiratory
activities. J. Aerosol Sci 40, 256–269 (2009).
39. Flint, S. J., acaniello, V. ., Enquist, L. W. & Sala, A. M. Principles of virology, Volume 2: pathogenesis and control, (ASM press,
2009).
40. eene, O. N. e log transformation is special. Sta t Med 14, 811–819 (1995).
41. Ihaa, . & Gentleman, . : a language for data analysis and graphics. J. Comp. Graph. Stat. 5, 299–314 (1996).
Acknowledgements
is work was supported by the Shostack Foundation and also NIH grant 1R41AI125006–01. We thank Dr. Rea
Dabelic from the Department of Environmental Health Sciences, Mailman School of Public Health at Columbia
University for her expertise and training with viral cell culture.
Author Contributions
D.W., M.B. and V.G. designed and performed experiments, analyzed the data, and wrote the manuscript; I.S.
analyzed the data; C.C. and A.W.B. designed the irradiation chamber; G.W.J. constructed the irradiation chamber;
D.J.B and G.R.-P. supervised, contributed conceptual advice, and wrote the manuscript. All authors discussed the
results and commented on the manuscript.
Additional Information
Competing Interests: The authors G.R.-P., D.J.B. and A.B. have a granted patent entitled ‘Apparatus, method
and system for selectively affecting and/or killing a virus’ (US10780189B2), that relates to the use of filtered
222 nm UV light to inactivate viruses. In addition, D.J.B. has an ongoing non-financial collaboration with
Eden Park Illumination, and the authors’ institution, Columbia University, has licensed aspects of UV light
technology to USHIO Inc.
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and
institutional aliations.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International
License, which permits use, sharing, adaptation, distribution and reproduction in any medium or
format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Cre-
ative Commons license, and indicate if changes were made. e images or other third party material in this
article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the
material. If material is not included in the article’s Creative Commons license and your intended use is not per-
mitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the
copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
© e Author(s) 2018, corrected publication 2021
Content courtesy of Springer Nature, terms of use apply. Rights reserved
1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com
Available via license: CC BY 4.0
Content may be subject to copyright.