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Ecotoxicology and Public Health

Expiratory Aerosol pH: The Overlooked Driver of Airborne Virus Inactivation
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  • Beiping Luo
    Beiping Luo
    Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland
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  • Aline Schaub
    Aline Schaub
    Environmental Chemistry Laboratory, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
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    Orcidhttps://orcid.org/0000-0002-1468-6678
  • Irina Glas
    Irina Glas
    Institute of Medical Virology, University of Zurich, CH-8057Zurich, Switzerland
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    Orcidhttps://orcid.org/0000-0001-6976-6360
  • Liviana K. Klein
    Liviana K. Klein
    Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland
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    Orcidhttps://orcid.org/0000-0002-7205-1718
  • Shannon C. David
    Shannon C. David
    Environmental Chemistry Laboratory, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
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    Orcidhttps://orcid.org/0000-0003-3345-9443
  • Nir Bluvshtein
    Nir Bluvshtein
    Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland
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    Orcidhttps://orcid.org/0000-0002-7999-4460
  • Kalliopi Violaki
    Kalliopi Violaki
    Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
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  • Ghislain Motos
    Ghislain Motos
    Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
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  • Marie O. Pohl
    Marie O. Pohl
    Institute of Medical Virology, University of Zurich, CH-8057Zurich, Switzerland
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  • Walter Hugentobler
    Walter Hugentobler
    Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
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    Orcidhttps://orcid.org/0000-0002-7379-752X
  • Athanasios Nenes
    Athanasios Nenes
    Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
    Institute of Chemical Engineering Sciences, Foundation for Research and Technology Hellas, GR-26504Patras, Greece
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    Orcidhttps://orcid.org/0000-0003-3873-9970
  • Ulrich K. Krieger
    Ulrich K. Krieger
    Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland
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    Orcidhttps://orcid.org/0000-0003-4958-2657
  • Silke Stertz
    Silke Stertz
    Institute of Medical Virology, University of Zurich, CH-8057Zurich, Switzerland
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    Orcidhttps://orcid.org/0000-0001-9491-2892
  • Thomas Peter*
    Thomas Peter
    Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland
    *Email: [email protected]
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  • Tamar Kohn*
    Tamar Kohn
    Environmental Chemistry Laboratory, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
    *Email: [email protected]
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    Orcidhttps://orcid.org/0000-0003-0395-6561
Open PDFSupporting Information (1)

Environmental Science & Technology

Cite this: Environ. Sci. Technol. 2023, 57, 1, 486–497
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https://doi.org/10.1021/acs.est.2c05777
Published December 20, 2022

Copyright © 2022 The Authors. Published by American Chemical Society. This publication is licensed under

CC-BY-NC-ND 4.0 .

Abstract

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Respiratory viruses, including influenza virus and SARS-CoV-2, are transmitted by the airborne route. Air filtration and ventilation mechanically reduce the concentration of airborne viruses and are necessary tools for disease mitigation. However, they ignore the potential impact of the chemical environment surrounding aerosolized viruses, which determines the aerosol pH. Atmospheric aerosol gravitates toward acidic pH, and enveloped viruses are prone to inactivation at strong acidity levels. Yet, the acidity of expiratory aerosol particles and its effect on airborne virus persistence have not been examined. Here, we combine pH-dependent inactivation rates of influenza A virus (IAV) and SARS-CoV-2 with microphysical properties of respiratory fluids using a biophysical aerosol model. We find that particles exhaled into indoor air (with relative humidity ≥ 50%) become mildly acidic (pH ∼ 4), rapidly inactivating IAV within minutes, whereas SARS-CoV-2 requires days. If indoor air is enriched with nonhazardous levels of nitric acid, aerosol pH drops by up to 2 units, decreasing 99%-inactivation times for both viruses in small aerosol particles to below 30 s. Conversely, unintentional removal of volatile acids from indoor air may elevate pH and prolong airborne virus persistence. The overlooked role of aerosol acidity has profound implications for virus transmission and mitigation strategies.

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Synopsis

Respiratory viruses are sensitive to aerosol pH, an unidentified factor in the mitigation of airborne virus transmission.

Introduction

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Respiratory viral infections pose a great burden on human health. An average of 400,000 deaths are associated with influenza globally each year, (1) and the ongoing COVID-19 pandemic has already resulted in several million deaths and countless cases of long COVID around the world. To curb the public health and economic impacts of these diseases, health care policy aims to minimize virus transmission. Increasing evidence points to expiratory aerosol particles (see ref (2) for clarification of terminology) as vehicles for the transmission of influenza virus and SARS-CoV-2. (3) The persistence of these viruses in aerosols is still subject to scientific debate, with prior studies reporting highly variable rates of viral inactivation depending on the study design and choice of matrix. (4−6) Regardless, it is undisputed that rapid inactivation would contribute to limiting their spread.
Prior studies have investigated the effect of ambient conditions on the inactivation rates of aerosolized respiratory viruses including influenza virus, (5,7−11) SARS-CoV-2, (12−14) and the common cold human coronavirus HCoV-229E. (15) Relative humidity (RH) and temperature were the primary variables modulated in these works, with low (∼20%), medium (40–60%), and high (65–90%) RH compared at a few select temperatures. Some of these studies identified a “U-shaped” curve of inactivation as a function of RH, (7,10) and it has been suggested that RH affects virus inactivation by controlling evaporation of water from the aerosol particle, thus governing the concentration of inactivation-catalyzing solutes. (16−18) Furthermore, the physical processes of efflorescence and deliquescence due to varying RH have been suggested to influence surviving viral fractions of respiratory viruses. (19,20) In addition, the role of matrix composition including its protective effects on virus inactivation has been investigated. (5,10,21) Beyond this, the mechanisms of virus inactivation in aerosol particles remain largely speculative.
A potentially powerful, yet understudied driver of airborne virus inactivation is the aerosol pH. It is established now that atmospheric aerosol particles can be highly acidic (22) and that some enveloped viruses, including influenza virus, are sensitive to low pH. (23) Nevertheless, even though previously hypothesized to be a determinant of virus fate, (24) the pH of expiratory aerosol particles, and hence its contribution to the inactivation of airborne viruses, remains poorly understood. The aerosol pH depends on the composition of the aerosol particle and the surrounding air, and it is well characterized for particulate matter equilibrated with inorganic acids and bases. (25) Recently, Oswin et al. (26) suggested that aerosol particles lose CO2 upon exhalation, and they argue that the resulting alkaline aerosol pH (∼10) may account for the moderate inactivation of SARS-CoV-2 observed in their experimental system. However, the impact of air composition beyond RH and CO2 has been overlooked to date. To the best of our knowledge, the only attempt to inactivate airborne viruses by modulating aerosol pH is the use of acetic acid from boiling vinegar during the 2002/03 outbreak of SARS-CoV-1 (see ref (27) and the Supporting Information).
Outdoor airborne particulate matter is often highly acidic, with pH values ranging between −1 and +5. (22,25) Contrary to expectations, the strength of the acid or base contained in aerosols (expressed by its dissociation constants) may not be the dominant parameter controlling aerosol pH. Rather, the volatility of species is of importance. For example, strong organic acids such as HCOOH and CH3COOH partition negligibly to aerosol and bear a minor impact on aerosol pH for most atmospherically relevant conditions. (28) In contrast, HNO3 and NH3 partition into aerosol particles and impact pH, albeit buffered by the formation of ammonium nitrate.
Indoor aerosol particles have a variety of sources, including ventilation with outdoor air and human emissions from the respiratory tract, skin, and clothing. Indoor air tends to have lower levels of gas-phase inorganic acids (e.g., HNO3) than outdoor air owing to their efficient removal via deposition on surfaces, as well as their condensation on indoor aerosol particles. Human activities are a source of organic acids and NH3, (25,29,30) often elevating their levels compared to outdoors. The ratio of indoor to outdoor concentrations is typically 0.1–0.5 for HNO3 and 3–30 for NH3, (30) causing the pH of indoor aerosol particles to increase compared to outdoor levels. Operation of humidification, ventilation, and air conditioning systems also affects air composition (31) and, hence, likely the pH of indoor aerosol particles. While many outdoor and indoor aerosol particles are in equilibrium with their environment, this can only be expected for exhaled aerosol if given enough time. In the interim, freshly exhaled aerosol can change its pH considerably.
Exhaled air, before mixing into the indoor air, contains high concentrations of NH3 and is characterized by very high concentrations of CO2 and high number densities of expiratory aerosol particles. These particles are emitted by breathing, talking, coughing, or sneezing and contain a complex aqueous mixture of ions, proteins, and surfactants. Although the pH of exhaled breath condensate has been investigated, such measurements are often performed after deaeration by bubbling a noble gas through the sample, which leads to the loss of CO2 and an increase of pH. (32) There is no study that quantifies the pH of respiratory aerosol when it equilibrates with the acidic or alkaline gases present in the indoor air within a few seconds to minutes of exhalation.
Here, we investigate the role of aerosol acidity in the inactivation of airborne influenza A virus (IAV) and two coronaviruses, SARS-CoV-2 and HCoV-229E, in indoor environments. We accomplish this in three steps by first determining the pH-dependent inactivation kinetics of IAV, SARS-CoV-2, and HCoV-229E in bulk samples of representative respiratory fluids, then measuring the thermodynamic and kinetic properties of microscopic particles of these fluids in an electrodynamic balance (EDB), and finally jointly applying the inactivation kinetics and aerosol properties in a biophysical model to determine inactivation in the aerosol system. We then use the model to investigate virus inactivation under a range of particle sizes and indoor air compositions. Finally, we assess the virus transmission risk under different interventions that modulate aerosol pH, including air filtration, NH3 scrubbing, or enrichment with nonhazardous concentrations of HNO3.

Materials and Methods

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Virus Inactivation Experiments

Experiments were conducted with three viruses [influenza virus strain A/WSN/33 (H1N1), SARS-CoV-2 strain BetaCoV/Germany/BavPat1/2020, and HCoV-229E-Ren] in three liquid matrices [synthetic lung fluid (SLF; see Table S1 for composition), mucus harvested from primary epithelial nasal cultures grown at the air–liquid interface (nasal mucus), or aqueous citric acid/Na2HPO4 buffer]. All details pertaining to virus propagation, purification, and enumeration, as well as to matrix preparation and composition, are given in the Supporting Information.
Virus inactivation curves were measured at room temperature in 2 mL glass vials (G085S-1-H; Infochroma), 500 μL PCR tubes (Sarstedt), or 1.5 mL plastic tubes (Eppendorf) using a matrix volume between 10 μL and 1 mL. Each experimental condition was tested in triplicate, except for a subset of SARS-CoV-2 experiments, which were performed in duplicate. IAV stock solutions were diluted with ultrapure distilled water (Thermo Fisher Scientific) to reach an approximate titer of 109 plaque forming units (PFUs)/mL. Virus stocks were then spiked into each test matrix to an initial experimental titer of 107 PFU/mL for IAV and HCoV-229E or 3 × 106 PFU/mL for SARS-CoV-2. After spiking, vials were vortexed at medium intensity for approximately 5 s, with the exception of SARS-CoV-2 samples, which were flick-mixed due to biosafety restrictions. The total exposure time was adjusted depending on the inactivation rate and ranged between 20 s for the lowest pH and 48 h for near-neutral pH. The sample pH stayed stable over the duration of the experiment. Samples were taken at regular time intervals (3 to 11 time points within each pH exposure) and were neutralized by diluting 1:100 in phosphate-buffered saline (PBS) for infection [PBSi; PBS containing 3% of bovine serum albumin solution 10% in DPBS (Sigma-Aldrich), 1% of P/S, and 1% of Ca2+/Mg2+ 100 mM (CaCl2·2H2O and MgCl2·6H2O, Acros Organics)]. The PBSi has a pH of 7.3. In most experiments with pH < 3.5, PBSi was supplemented with 2% of 10× citric acid–phosphate buffer at pH 7. Dilution in PBSi rather than addition of a strong base was chosen for sample neutralization because the latter approach was found to further decrease the virus titer. Neutralized samples were frozen until enumeration. To determine kinetic parameters, all replicate experiments of a given experimental condition were pooled. Inactivation rate constants were determined from least-square fits to the log-linear portion of the inactivation curves, assuming pseudo-first order kinetics
ln⁡CC0=−kobs·t
(1)
Here, C is the virus titer at time t, C0 is the initial virus titer, and kobs is the observed inactivation rate constant. For measurements of C below the limit of detection (LoD), C was set to the LoD value. 99%-inactivation times (t99) were determined based on kobs
t99=−ln(0.01)kobs
(2)
Rate constants and associated 95% confidence intervals were determined using GraphPad Prism v.9.232. Control experiments were performed to confirm that virus titer loss at low pH could not be attributed to virus aggregation (Figure S1).

EDB Measurements of Aerosol Thermodynamics and Diffusion Kinetics

An EDB setup was used to measure the thermodynamic and kinetic properties of SLF and nasal mucus. The EDB measures the relative changes in mass and size of a single levitated particle as a result of changing RH; our specific setup is described in previous publications. (33,34) To generate the particles, we used concentrated SLF (1 mL of freeze-dried SLF in 400 μL of Millipore water) and freshly thawed nasal mucus. Briefly, a charged SLF/mucus droplet is injected with a droplet on demand generator (HP ink jet) into an environmental chamber (288.15 K) and levitated by an adjustable electric field. (35) The particle experiences two forces along the symmetry axis of the EDB: a gravitational force and a drag force induced by the gas flow through the chamber. Therefore, the DC voltage required to balance the particle in the center of the EDB is sensitive to the loss or uptake of water vapor. To induce gas-particle partitioning of water vapor at or near-equilibrium conditions, the RH in the chamber was slowly cycled between dry (<5%) and humid (ca. 90%) conditions by mixing dry and humidified N2 flows. More rapid changes in RH allow inferring mass-transfer limitations by observing a delayed particle response. (36) The total flow was set to 20 sccm and controlled by mass flow controllers. The RH was measured with a capacitance sensor which is calibrated observing the deliquescence of various salts. Its accuracy was estimated to be ±1.5%. The particle size was determined by analyzing Mie resonances apparent in continuously recorded broad-band back scattering spectra. (34,37,38) The initial radius was estimated at 91% RH utilizing the resonance structure of Mie scattering. (39) An extended description of the EDB approach and data processing is given in the Supporting Information.

Biophysical Modeling

The Respiratory Aerosol Model ResAM is a biophysical model to determine virus inactivation times in the exhalation aerosol as a function of air composition. ResAM is based on a spherical shell diffusion model, which we have previously applied in physical and chemical contexts. (36,40,41) As novel input experimental data, ResAM uses the pH sensitivity of enveloped viruses and the thermodynamic and kinetic properties of respiratory fluids, both measured in the present work.
ResAM simulates the composition and pH changes inside an expiratory particle during exhalation. Hereby, we make the simplifying assumption that the mode of generation (breathing, coughing, and singing) does not influence the matrix composition. The model performs calculations for particles of selectable size (from 25 nm to 1 mm) with a liquid composed of H2O, H+, OH–, Na+, Cl–, CO2(aq), HCO3–, NH3(aq), NH4+, CH3COOH(aq), CH3COO–, CH3COONH4(aq), NO3–, as well as two classes of organic compounds with low and high molecular weight, representative of the lipids and proteins in the lung fluid (see subsection “Species treated by ResAM” in the Supporting Information for details).
The liquid phase is divided into concentric shells (Figure S2). The model treats 1–50 shells, depending on particle size (one shell for r = 0.02–0.1 μm and up to 50 shells for r = 1000 μm). The number of shells for each particle stays constant during the exhalation process. The shells are treated in a fully Lagrangian manner, that is, their thicknesses are calculated from the number of molecules of each species in a shell times their molecular volume, whereby diffusion processes between shells may cause each shell to evolve differently with time. By allowing the thickness of the shells to change, mass conservation is well satisfied (see the Supporting Information).
We take account of vapor pressures pH2Ovap, pNH3vap, pHClvap, pHNO3vap, and pCH3COOHvap calculated using Henry’s law coefficients listed in Table S2. The activity coefficients of H+, Na+, Cl–, NO3–, and OH– required for the vapor pressure and concentration simulation are calculated using the Pitzer ion-interaction model. (42,43) The activity coefficients of organic and neutral species are assumed to be unity, that is, they influence the physicochemical properties of SLF as ideal components simply via Raoult’s law. SLF contains additional ions in minor concentration (Table S1). For all other minor anions, the activity coefficients of Cl– and for the cations the activity coefficients of Na+ are used. We obtain the liquid-phase diffusion coefficients of ionic and neutral species as well as the efflorescence RH values from our EDB measurements, assuming that the virus does not affect these properties [as preliminary experiments confirm (not shown)]. The liquid-phase diffusion coefficients Dl of the involved species in water are given in Table S3. In the absence of other information, we assume that Dl of all neutral species has the same dependence on water activity (aw) as Dl,H2O(aw) scaled with their value at infinite dilution. Similarly, the diffusivities of cations and anions are assumed to have the same dependence on aw as Na+ and Cl–, respectively, again scaled with their dilute solution values from the literature. When RH decreases below efflorescence RH, we assume the resulting NaCl crystal to reside in the particle center and parameterize the effects of nonspherical symmetries, such as dendritic crystal growth, in terms of effective diffusivities (see more details on the related uncertainties in the Supporting Information).
We then use the model to calculate the pH value, and from this the corresponding virus inactivation rates, in each particle shell. The gas-phase compositions of exhaled air and the indoor air with purification and acidification are shown in Table S4. A detailed description of the ResAM model and its application to estimate virus inactivation and transmission risks is given in the Supporting Information. The current version of ResAM can readily be further refined beyond the conditions used herein, for example, to include a greater diversity of respiratory matrices or additional atmospheric gases.

Results and Discussion

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Kinetics of pH-Mediated Inactivation of Influenza Virus and Coronavirus

Inactivation kinetics of IAV, SARS-CoV-2, and HCoV-229E were determined over a pH range from neutral to strongly acidic after immersion in bulk solutions of SLF, nasal mucus, or aqueous buffer. Figure 1 summarizes the inactivation times (here expressed as the time to reach a 99% infectivity loss) as a function of pH. All viruses were stable in all matrices at neutral pH, with inactivation times of several days. From pH 6 to 4, IAV inactivation times decreased from days to seconds or by about 5 orders of magnitude. This decrease was evident in all matrices studied. It is noteworthy that inactivation in nasal mucus, which is most representative of the matrix comprising expiratory aerosol particles, is well described by SLF. However, inactivation times did depend on the SLF concentration. Specifically, we determined IAV inactivation at three different levels of SLF enrichment (1× and 18× SLF, determined experimentally; 24× SLF, determined by concentration-proportional extrapolation), corresponding to water activities aw = 0.994, 0.8, and 0.5. This represents the fluid in equilibrium with a gas phase at 99.4, 80, and 50% RH, that is, from physiological equilibrium to common indoor conditions. The study of Lin et al. (44) suggests that the protective effect of proteins in the case of bacteriophages is concentration-proportional at high RH (80%) but is not as effective at lower RH (20–50%). Therefore, we assume that the concentration-proportional extrapolation is reasonable and might even become an overestimation at low RH. While inactivation times in aqueous buffer, 1× SLF, and nasal mucus were very similar, 18× enrichment of the SLF coincided with an increase in inactivation time by up to a factor of 56 (blue triangles in Figure 1). This protective effect of concentrated SLF was most prominent around the optimal pH for A/WSN/33 viral fusion of 5.1. (45) Coronaviruses were less affected by acidic pH than IAV. Both SARS-CoV-2 and HCoV-229E remained largely stable down to pH 3, where their inactivation still required 24 h. When further decreasing pH down to 2, the inactivation times rapidly reduced to <10 s for SARS-CoV-2 but never dropped below 2 h for HCoV-229E. Compared to aqueous buffer, SLF provided some protection against inactivation below pH 3, both at 1× and 5× SLF concentrations (while measurements for pH < 3 in 18× SLF were not possible due to precipitation). The measured differences in pH sensitivities between IAV and the coronaviruses may be explained by their different mechanisms of virus entry into host cells. IAV relies on an acid-induced conformational change in haemagglutinin during endosomal entry. This conformational change is irreversible; (46) if IAV encounters the fusion pH (typically pH < 5.5) outside the host cell, for example, while within an aerosol particle, the acid-triggered haemagglutinin can no longer bind to host-cell receptors and the virus is inactivated. Notably, IAV strains vary in their fusion pH optima (45) and therefore might also differ in their inactivation dynamics. Conversely, the spike glycoprotein of coronaviruses becomes fusion competent through cleavage by host proteases, instead of relying on acidic pH triggering conformational changes. (47) The different behavior of SARS-CoV-2 and HCoV-229E at pH < 3 remains unclear.

Figure 1

Figure 1. Time required for 99% titer reduction of IAV, SARS-CoV-2, and human coronavirus HCoV-229E in various bulk media. Data points represent inactivation times in aqueous citric acid/Na2HPO4 buffer, SLF, or nasal mucus with pH between 7.4 and 2, measured at 22 °C. SLF concentrations correspond to water activity aw = 0.994 (1× SLF; squares), aw = 0.97 (5× SLF; stars), and aw = 0.8 (18× SLF; triangles); buffer (circles) and nasal mucus (diamonds) correspond to aw ≈ 0.99. Each experimental condition was tested in replicate with error bars indicating 95% confidence intervals. While IAV displays a pronounced reduction in infectivity around pH 5, SARS-CoV-2 develops a similar reduction only close to pH 2, and HCoV-229E is largely pH-insensitive. Solid lines are arctan fits to SLF data with aw = 0.994 (blue: IAV; red: SARS-CoV-2; and black: HCoV-229E; see eqs S26–S28). The dashed line is an arctan fit to the SLF data with aw = 0.80. The dotted line is a concentration-proportional extrapolation to aw = 0.5 (24× SLF). Upward arrows indicate insignificant change in titer over the course of the experiment, and downward arrows indicate inactivation below the level of detection at all measured times. The fitted curves below pH 2 (gray shaded area) are extrapolated with high uncertainty. Examples of measured inactivation curves are shown in Figure S3.

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Thermodynamics and Diffusion Kinetics of Expiratory Particles

While Figure 1 shows the pH that must be attained in the aerosol particles for rapid virus inactivation, it lacks information on aerosol particle pH after exhalation into indoor air. To model the pH in these particles, it is essential to know the particle composition in thermodynamic equilibrium (liquid water content), as well as the kinetics that determine how rapidly the equilibrium is approached (water and ion diffusion coefficients). To obtain this information, we measured thermodynamic (equilibrium) and kinetic (diffusion-controlled) properties of individual micrometer-sized SLF and nasal mucus particles levitated contact-free in an EDB. Each particle was exposed to prescribed changes in RH (see Figure 2). Figure 2A shows two moistening/drying cycles of an SLF particle obtained over a period of 2 days. They allow determination of the particle equilibrium composition (water content or mass fraction of solutes, see Figure S4A) during time intervals with slowly changing RH. The particle clearly takes up and loses water when the RH is changed. It has a size growth factor at 90% RH of 1.3 (see also Figure S5) and deliquesces at 75%, indicating that NaCl is the predominant salt in the particle. Nasal mucus shows a similar size growth but deliquesces at 69% RH, indicating that it contains significant amounts of other hygroscopic compounds (Figure S5). We have no evidence for liquid–liquid phase separation in any of these particles (Figures S6A and S7), but Mie-resonance spectra indicate inhomogeneities in the particles even at high RH.

Figure 2

Figure 2. Measured hygroscopicity cycles of an SLF particle in an EDB forced by prescribed changes in RH. The voltage required to balance the particle in the EDB against gravitational settling and aerodynamic forces is a measure of the particle’s mass-to-charge ratio, allowing the particle radius R to be estimated. (A) Two humidification cycles of an SLF particle with a dry radius R0 ≈ 9.7 μm. The experiment spanned about 2 days with slow humidity changes, allowing the thermodynamic and kinetic properties of SLF to be determined. Deliquescence/efflorescence points are marked by “Deliq/Effl”. (B) Zoom on the drying phase [red box in (A)] with salts in the droplet (mainly NaCl) efflorescing around 56% RH (black line): very fast initial crystal growth (<10 s) with rapid loss of H2O from the particle, followed by slow further crystal growth (1 h). The latter is caused by the abrupt switch from H2O diffusion to the diffusion of Na+ and Cl– ions through the viscous liquid, resulting in an ion diffusion coefficient of Dl,ions* ≈ 10–10 cm2/s. The inset (C) highlights the minute before and after efflorescence, which allows a lower bound of the H2O diffusivity to be determined, namely, Dl,H2O > 10–7 cm2/s.

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The kinetics of water uptake/loss as derived from periods with rapid RH change or efflorescence are highlighted in Figure 2. Figure 2B zooms in on one efflorescence event, first showing rapid water loss (<10 s) and then switching to a much slower rate of water loss over the next hour. This two-stage diffusion process was confirmed in measurements of additional SLF and nasal mucus particles (see Figure S8). We interpret this as fast initial dendritic growth of an NaCl crystal (Figure S6A–C), which depends on the ability of H2O molecules to rapidly leave the particle and ends abruptly when the crystal reaches the droplet surface, followed by a slow crystal growth mode (Figure S6D), for which the diffusivity of the ions is crucial. In this representation, crystal growth is initially limited by the liquid-phase diffusivity of water molecules with Dl,H2O> 10–7 cm2/s (Figure 2C), which are expelled from the particle as long as water activity is still high. Subsequently, the slow crystal growth is limited by the diffusivities of Na+ and Cl– ions through the progressively viscous liquid to the crystal (Figure S6D). From Figures 2B and S6D, we estimate the ion diffusion coefficient to be about Dl,ions* ≈ 10–10 cm2/s, suggesting a viscous state which slows virus inactivation. While SLF and nasal mucus do not completely suppress the diffusivity of water molecules themselves (see Figure S9D), the very slow diffusion of the Na+ and Cl– ions keeps the concentration of the solution high and, thus, also determines the low rate of continued loss of water molecules. It should further be noted that the diffusion coefficients determined in this way are “effective” (indicated by a star) as they represent the molecular diffusivities under the specific morphological conditions associated with the dendritic growth of the salt crystals inside the droplets (see the next section for details on how these diffusion coefficients were further constrained).
Independent of the exact thermodynamic equilibrium state of the particles, our results demonstrate that SLF and nasal mucus show a clear diffusion limitation for ions. In contrast, water diffusion in SLF and nasal mucus remains fast even when RH is low. This continuous, rapid diffusion of water indicates that SLF and nasal mucus do not form diffusion-inhibiting, semisolid-phase states such as those recently reported by others in particles containing model respiratory compounds. (48)

Biophysical Model of Inactivation in Expiratory Aerosol Particles

The combination of the virological bulk-phase data (Figure 1) with the microphysical aerosol thermodynamics (vapor pressures and activity coefficients) and kinetics (Figures 2 and S9) allows the pH attained in the aerosol particles and the resulting rates of viral inactivation to be determined. Thus, the virological and microphysical data were combined as input for a multishell ResAM. ResAM is a biophysical model that simulates the composition and pH changes inside an expiratory particle during exhalation and determines the impact of these changes on virus infectivity (see the section “Biophysical Modeling” and the Supporting Information). The model performs calculations for particles of selectable size (from 20 nm to 1 mm) with a liquid phase composed of organic and inorganic species representative of human respiratory fluids (see Table S1). It takes account of diffusion in the gaseous and condensed phase, vapor pressures, heat transfer, deliquescence, efflorescence, species dissociation, and activity coefficients due to electrolytic ion interactions (see Tables S2 and S3). Ultimately, ResAM computes the species distribution and their activity in the liquid, the resulting pH, and the corresponding virus inactivation rates as a function of time and of the radial coordinate within the particle. A thorough discussion of uncertainties and validity limitations of the combined virus inactivation data from bulk-phase measurements, the aerosol microphysics determined in the EDB, and the multishell biophysical model is provided in the Supporting Information.
When RH changes are slow, the measured mass fraction of solutes in SLF as a function of RH allows the model thermodynamics to be constrained (Figure S4B). Under thermodynamic equilibrium conditions, the model captures the mass fraction of solutes along the deliquesced and effloresced branches of the particle reasonably well. However, only after kinetic effects (ion and water diffusivities) are also taken into account does the model accurately reproduce the solute composition curve along the deliquesced branch. This demonstrates that even when RH changes are slow (raising RH from 50 to 70% in over 1 h), kinetics cannot be neglected.
For rapidly evaporating expiratory particles, kinetic effects are even more critical. By matching the model to the fast changes during the efflorescence and deliquescence processes, ion diffusion coefficients can be derived for different water activities. Interpolation together with literature data under dilute conditions yields Dl,H2O, Dl,Na+, and Dl,Cl− (for details, see Figure S9D). Other neutral species, cations and anions, are treated accordingly, scaled with their infinite dilution values (see the Supporting Information).
As an example, Figure 3 shows the evolution of the physicochemical conditions within an expiratory particle with 1 μm initial radius during transition from nasal to typical indoor air conditions with 50% RH (see trace gases in Table S4) and the concomitant inactivation of IAV and SARS-CoV-2 contained within the particle. The rapid loss of water leads to concentration of the organics and salts to the point when NaCl effloresces. In addition to H2O, CO2, which stems from the dissolved bicarbonate, also evaporates from the particle, causing the pH to rise for a short time (<0.3 s) from the initial 6.6 to around 7.0. This is similar to the trend to higher pH observed by Oswin et al. (26) for much larger particles. However, this effect is only intermediate. (49) Nitric acid from the indoor air enters the particle readily, lowering its pH to 5 within ∼10 s. This, in turn, pulls NH3 into the particle, partly compensating the acidification. The pH further decreases to ∼4 within 2 min and then slowly approaches pH 3.7 due to further uptake of HNO3 from the room air. This result confirms the importance of trace gases in determining the pH of indoor aerosol particles. (30) If only CO2 is considered, its volatilization from the particle would lead to an expected increase in pH after exhalation. (26) Owing to aerosol acidification, rapid influenza virus inactivation occurs at ∼2 min, whereas SARS-CoV-2 (and the even more pH-tolerant HCoV-229E) remains infectious.

Figure 3

Figure 3. Evolution of physicochemical conditions within a respiratory particle leading to inactivation of trapped viruses during the transition from nasal to typical indoor air conditions, modeled with ResAM. The initial radius of the particle is 1 μm. Thermodynamic and kinetic properties are those of SLF (see Figure 2 and Table S1). The indoor air conditions are set at 20 °C and 50% RH (see Figure S10 for the corresponding depiction of physicochemical conditions at 80% RH). The exhaled air is assumed to mix into the indoor air using a turbulent eddy diffusion coefficient of 50 cm2/s (see Supporting Information, section “Mixing of the exhaled aerosol with indoor air”). The temporal evolution of gas-phase mixing ratios is shown in Figure S11. The gas-phase compositions of exhaled and typical indoor air are given in Table S4. Within 0.3 s, the particle shrinks to 0.7 μm due to rapid H2O loss, causing NaCl to effloresce (gray core). The particle then reaches 0.6 μm within 2 min due to further crystal growth, after which it slowly grows again due to coupled HNO3 and NH3 uptake and HCl loss. ResAM models the physicochemical changes in particles including (A) water activity, (B) molality of organics, (C) NO3– (resulting from the deprotonation of HNO3), (D) molality of total ammonium, (E) molality of Cl–, (F) pH, as well as inactivation of (G) IAV and (H) SARS-CoV-2 (decadal logarithm of virus titer C at time t relative to initial virus titer C0).

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Inactivation times vary with particle size: larger droplets take longer to reach low pH than smaller ones as they are impeded by longer diffusion paths of the relevant molecules (mainly HNO3 and NH3) or ions through both air and liquid phases. The black line in Figure 4D illustrates this relationship for IAV, showing 99% inactivation after about 2 min in particles with radii <1 μm but longer than 5 days for millimeter-sized particles. As a rule of thumb, a 10-fold increase in particle size leads to roughly a 10-fold increase in IAV inactivation time under typical indoor conditions. Conversely, the black line in Figure 4E for SARS-CoV-2 shows that inactivation is inefficient for SARS-CoV-2, irrespective of particle size.

Figure 4

Figure 4. Impact of airborne acidity on virus inactivation in expiratory particles. (A) Modeled pH value in a particle with properties of synthetic lung fluid with initially 1 μm radius exhaled into air (20 °C, 50% RH) with typical indoor composition (same as Figure 3F). (B) Same as (A), but for indoor air with NH3 reduced to 10 ppt, e.g., by means of an NH3 scrubber, reducing the time to reach pH 4 from 2 min to less than 10 s. (C) Same as (A), but in indoor air enriched to 50 ppb HNO3, reducing the time to reach pH 4 from 2 min to less than 0.5 s. (D,E) Inactivation times of IAV and SARS-CoV-2 as a function of particle radius under various conditions: indoor air with typical composition (black), depleted in NH3 to 10 ppt (light blue), enriched to 50 ppb HNO3 (dark blue), or purified air with both, HNO3 and NH3, reduced to 20 or 1% of typical indoor values (red). Whiskers show reductions of virus load to 10–4 (upper end), 10–2 (intersection with line), and 1/e (lower end). The exhaled air mixes with the indoor air by turbulent eddy diffusion (same as Figure 3); for sensitivity tests on eddy diffusivity, see Figures S14B and S15B. The gas-phase compositions of exhaled air and the various cases of indoor air shown here are defined in Table S4. (F) Mean size distribution of number emission rates of expiratory aerosol particles [dQ/dlog(R)] for breathing (solid line), speaking and singing (dotted line), and coughing (dashed line). (57) Dark gray range indicates virus radii. Light gray shading shows conditions for particles smaller than a virus, referring to an equivalent coating volume with inactivation times indicated. [Radius values in (D–F) refer to the particle size 1 s after exhalation].

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Inactivation times for both IAV and SARS-CoV-2 can be greatly reduced if the indoor air is slightly acidified. This can be achieved by either removing basic gases or adding acidic ones, provided that the gaseous acid molecules meet two conditions: their volatility must be sufficiently low, such that they readily partition from the gas phase to the condensed phase, and once dissolved, they must be sufficiently strong acids to overcome any pH buffering by the particle matrix. Figure 4 compares the aerosol pH in typical indoor air (panel A; NH3 = 36.3 ppb and HNO3 = 0.27 ppb) with that in air depleted in NH3 to 10 ppt (panel B) or enriched to 50 ppb HNO3 (panel C). This concentration of HNO3 is well below legal 8 h exposure thresholds (0.5–2 ppm (50,51)).
Scrubbing of NH3 reduces the time to reach an aerosol pH of 4 from minutes to seconds. Correspondingly, IAV inactivation times decrease by up to an order of magnitude (light blue lines in Figure 4D,E). This acceleration is mostly limited to particles in the 2–5 μm size range, which are minor contributors to the exhaled aerosol (Figure 4F). Furthermore, NH3 scrubbing does not affect SARS-CoV-2 inactivation because the aerosol pH remains in this virus’ stability range (Figure 1).
A much stronger effect is observed for the addition of HNO3. A HNO3 concentration of 50 ppb allows the aerosol pH value to drop below 2, which is required for efficient SARS-CoV-2 inactivation (Figure 1). For comparison, enriching air with the more volatile and weaker acetic acid at concentrations below exposure threshold values could not achieve this, see Figure S12. The dark blue lines in Figure 4D,E show the resulting inactivation times for IAV and SARS-CoV-2 (and Figure S13 for HCoV-229E) as a function of particle radius. Remarkably, inactivation times of SARS-CoV-2 diminished by 4–5 orders of magnitude compared to typical indoor air (black lines). For particles with radii <1 μm, which constitutes the majority of expiratory particles (see panel F), inactivation is expected to occur within 30 s.
While enrichment of acidic gases in air leads to an acceleration of IAV and SARS-CoV-2 inactivation, depletion of these gases, for instance by filtering freshly supplied air, has the opposite effect. It is well-known that concentrations of strong inorganic acids, such as HNO3, are lower indoors than outdoors by at least a factor of 2 and in buildings with special air purification, such as museums and libraries, by factors 10–80. (30) If air is purified to contain only a fraction of the initial trace gas concentrations (see Table S4), the aerosol pH increases compared to typical indoor air and intermittently reaches neutral or even slightly alkaline values (up to pH 8.4 in particles with 5 μm radius in air purified to 1%). As a result, air purification is expected to enhance virus persistence, especially for IAV, as indicated by the red curves in Figure 4D,E.
To validate the model results, we compared published inactivation data for aerosolized IAV and SARS-CoV-2 obtained in rotating drum experiments with inactivation times estimated by ResAM (Figures S16 and S17 and the Supporting Information). Even though rotating drums rely on time-integrated samples and are therefore not ideally suited to measure very rapid inactivation kinetics, modeled and measured inactivation times for both viruses exhibit similar trends as a function of RH. For IAV, measured inactivation times are consistent with ResAM predictions for experiments conducted in partly purified air, as is expected for rotating drum experiments. The comparison with SARS-CoV-2 is inconclusive because of the wide scatter in the experimental data. However, ResAM predictions fall within the range of measured inactivation times. Given the importance of semivolatile acids and bases for inactivation, further model validation should include inactivation times measured in aerosol experiments under well-known air compositions, including the presence of HNO3.

Management of Airborne Transmission Risks

Given the high pH sensitivity of many viruses (23,52−54) and the readiness of expiratory aerosol particles for acidification, we next investigated the extent to which the modification of indoor air composition could mitigate the risk of virus transmission. To this end, we consider a ventilated room with occupants who exhale aerosol containing infectious viruses. We further make the assumption that, given the low concentration of airborne viruses, the transmission risk is directly proportional to the infectious virus concentration, respectively, in inhalation dose. We use the term “relative risk of transmission” to express how the risk changes from standard conditions (here, typical indoor air according to Table S4) compared to air slightly enriched by HNO3, scrubbed of NH3, or air that has been purified.
For the ventilated room, we assume steady-state conditions where the exhalation defines the source of virus, which is balanced by three sinks, namely, air exchange through ventilation, aerosol deposition, and pH-moderated virus inactivation within the aerosol particles (see the Supporting Information). We describe the virus source by the mean size distributions of number emission rates of expiratory aerosol particles (Figure 4F) and assume each particle with radius >50 nm to carry one virus irrespective of size (see Figure S18 for a sensitivity test relaxing this assumption). We describe the virus sinks by expressing ventilation by air change per hour (ACH, mixing ventilation), applying mean aerosol deposition rates, (55) and computing the inactivation rates as for Figure 4D,E. This allows the airborne viral load and, thus, the relative risk of transmission to be calculated, as displayed in Figure 5 for IAV and SARS-CoV-2 (and Figure S19 for HCoV-229E). Black bars show the results for typical indoor conditions, light blue bars indicate air from which NH3 was scrubbed to 10 ppt, dark blue bars an enrichment of HNO3 to 50 ppb, and red bars indicate purification of air to 20 or 1% of trace gases (see Table S4).

Figure 5

Figure 5. Airborne viral load (# infectious viruses per volume of air) and relative risk of IAV (A) and SARS-CoV-2 (B) transmission under different air treatment scenarios. Calculations are for a room (20 °C, 50% RH) with different ventilation rates (ACH) and subject to various air treatments, assuming the room to accommodate one infected person per 10 m3 of air, emitting virus-laden aerosol by normal breathing (solid curve in Figure 4E), and assuming one infectious virus per aerosol particle irrespective of size (see Figure S18 for a scenario with a size-dependent virus distribution). Steady-state viral load (left axes) is calculated as the balance of exhaled viruses and their removal by ventilation (0.1–10 ACH), deposition, and inactivation (calculated as for Figure 4D,E, starting from radius 0.05 μm, the radius of viruses). ACH affects the indoor trace gas-phase concentrations [at higher ACH, gases with predominantly outdoor sources (HNO3 and HCl) have higher concentration and gases with indoor sources (NH3, CO2, and CH3COOH) have lower concentrations]. We assume gas-phase concentrations in Table S4 to refer to 2 ACH and then calculate the gas-phase concentration for 10 ACH and 0.1 ACH by mixing with more or less outdoor air (see the Supporting Information for further details). ACH also determines the mixing speed of the exhalation plume with indoor air (see the Supporting Information). Whiskers show the uncertainty range resulting from the spread of trace gas concentrations in room air (upper limits use the least acidic composition in Table S4, i.e., the highest measured NH3 and the lowest for all acidic gases and lower limits conversely). Right axes show the transmission risk under these treatments relative to the risk in a room with typical indoor air (see Table S4) and 2 ACH (thin horizontal line). A detailed description of the relative risk calculations is given in the Supporting Information. Typical indoor air is shown by black bars, filtered air with removal of trace gases to 20% or to 1% by red bars, air with NH3 removed to 10 ppt by light blue bars, and air enriched to 50 ppb HNO3 by dark blue bars. The whiskers in the case with NH3 removal include the range of possible HNO3 release from the background aerosol particles after removing NH3 from the indoor air (see Table S4). Thick gray horizontal lines indicate the viral load and relative transmission risk in the absence of any inactivation. Results for 2 and 5 ppb HNO3, see Figure S20, results for HCoV-229E, and analyses for coughing and speaking/singing, see Figure S19.

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Figure 5 highlights the importance of ventilation, which does not only lead to a dilution of the viral load but in addition has the important role of resupplying acidic gases from outside. A further improvement is reached by enriching HNO3 to 50 ppb, which diminishes the relative risk of transmission of IAV by a factor of ∼80 and of SARS-CoV-2 by a factor of ∼1000 in rooms with 2 ACH. Interestingly, HNO3 addition outperforms an increase in ventilation from 2 ACH to 10 ACH. Notably, inactivation times of IAV and SARS-CoV-2 drop to only a few seconds for small particles (Figure 4D,E) and are now on the same time scale as HNO3 transport through the gas phase to the droplet by ACH-induced eddy diffusion (see the Supporting Information). In this scenario, higher ACH leads to a faster mixing of the HNO3-enriched air into the exhaled plume, resulting in faster acidification of the exhaled aerosol, and hence a lower relative risk of transmission at higher ACH (dark blue bars in Figure 5). In contrast, enrichment to 50 ppb HNO3 only has a moderate impact on HCoV-229E (Figures S13 and S19).
In comparison, NH3 scrubbing reduces the relative risk of IAV transmission by a factor of 2–3, depending on the human activity (Figures S19 and S18). This approach, however, is ineffective for SARS-CoV-2 or HCoV-229E, highlighting the importance of ventilation in such a scenario.
Finally, the ResAM estimates for purified air with significant reduction of trace gases (red bars) are also striking. While even normal air conditioning systems with air filters can lead to a reduction in “sticky” molecules such as HNO3, (56) acid removal is likely even more pronounced in museums, libraries, or hospitals with activated carbon filters. (30) In such public buildings, the relative risk of IAV transmission can increase significantly compared to buildings supplied with unfiltered outdoor air.
In summary, we demonstrate that the control of aerosol pH is a critical tool in the mitigation of airborne virus transmission. We predict that a significant abatement in transmission risk can be achieved by air acidification and we are currently working to validate this prediction in aerosol experiments. For strongly pH-sensitive viruses (e.g., IAV), mere scrubbing of NH3 from indoor air suffices to bring about a modest reduction in the airborne viral load. A greater effect that also extends to more acid-tolerant viruses (e.g., SARS-CoV-2) results from air enrichment with an acidic gas. Here, we evaluated the use of HNO3 for this purpose because it is already ubiquitous in the outdoor environment, even though alternative acids may achieve similar results and may enjoy higher user acceptability. An effective reduction in viral load can already be achieved by applying HNO3 at levels lower than 10% of the legal exposure thresholds. (50,51) We therefore expect that the resulting acid exposure will not cause harmful effects on human health. Nevertheless, future studies should investigate the consequences of acid accumulation in indoor air on the microbiome and immune response in the respiratory tract. Additionally, methods are needed for real-time monitoring of aerosol pH, both to prevent acid overexposure and to ensure efficient virus inactivation. Also, finally, successful virus control through air acidification will also require educating the public about the value of adopting appropriate measures for indoor air quality. Nevertheless, even if acidification is never adopted owing to these concerns, the arguments toward ammonia stripping─which in itself may be sufficient to inactivate influenza virus rapidly─is an indirect way to increase acidity and allow acidic gases occurring in the environment to maximize their impact.
Despite the current unknowns, targeted regulation of aerosol pH promises profound positive effects on airborne virus control. Practices that help acidify exhaled aerosols should thus be considered as a strategy to mitigate virus transmission and disease─alongside interventions such as ventilation that mechanically reduce the concentration of airborne viruses (i.e., dilution) and ensure the resupply of acid molecules from outdoor air.

Supporting Information

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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.2c05777.

  • Method descriptions for virus and matrix preparation, measurement of viral aggregates and electron microscopy for SLF characterization; further details for EDB measurements; in-depth description of ResAM, its uncertainties, and limitations; descriptive comparison of ResAM results with published data; investigation of acetic acid as a potential agent against airborne viruses; particle-shell model; extent and effect of virus aggregation at low pH and high ionic strength; exemplary inactivation curves; additional EDB measurements; (electron) microscopy images of SLF; evolution of physicochemical conditions within aerosols at 80% RH; modeled inactivation times in the presence of acetic acid; modeled inactivation times of HCoV-229E; ResAM sensitivity study results; visual comparison of literature inactivation data and ResAM results; viral load and transmission risk for breathing, coughing, and singing at different air compositions and ventilation rates; substantiation of the assumptions of the ResAM model; composition of SLF; equilibrium constants; liquid-phase diffusion coefficients; and air compositions used in the ResAM model (PDF)

Terms & Conditions

Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Author Information

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  • Corresponding Authors
    • Thomas Peter - Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland;  Email: [email protected]
    • Tamar Kohn - Environmental Chemistry Laboratory, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland;  Orcidhttps://orcid.org/0000-0003-0395-6561;  Email: [email protected]
  • Authors
    • Beiping Luo - Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland
    • Aline Schaub - Environmental Chemistry Laboratory, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland;  Orcidhttps://orcid.org/0000-0002-1468-6678
    • Irina Glas - Institute of Medical Virology, University of Zurich, CH-8057Zurich, Switzerland;  Orcidhttps://orcid.org/0000-0001-6976-6360
    • Liviana K. Klein - Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland;  Orcidhttps://orcid.org/0000-0002-7205-1718
    • Shannon C. David - Environmental Chemistry Laboratory, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland;  Orcidhttps://orcid.org/0000-0003-3345-9443
    • Nir Bluvshtein - Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland;  Orcidhttps://orcid.org/0000-0002-7999-4460
    • Kalliopi Violaki - Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
    • Ghislain Motos - Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland
    • Marie O. Pohl - Institute of Medical Virology, University of Zurich, CH-8057Zurich, Switzerland
    • Walter Hugentobler - Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland;  Orcidhttps://orcid.org/0000-0002-7379-752X
    • Athanasios Nenes - Laboratory of Atmospheric Processes and Their Impacts, School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), CH-1015Lausanne, Switzerland;  Institute of Chemical Engineering Sciences, Foundation for Research and Technology Hellas, GR-26504Patras, Greece;  Orcidhttps://orcid.org/0000-0003-3873-9970
    • Ulrich K. Krieger - Institute for Atmospheric and Climate Science, ETH Zurich, CH-8092Zurich, Switzerland;  Orcidhttps://orcid.org/0000-0003-4958-2657
    • Silke Stertz - Institute of Medical Virology, University of Zurich, CH-8057Zurich, Switzerland;  Orcidhttps://orcid.org/0000-0001-9491-2892
  • Author Contributions

    B.L., A.S., I.G., and L.K.K. contributed equally to this work. Conceptualization: A.N., S.S., T.K., T.P., U.K.K., and W.H. Methodology: A.S., B.L., I.G., L.K.K., M.O.P., N.B., S.C.D., S.S., T.K., T.P., and U.K.K. Investigation: A.S., B.L., I.G., K.V., L.K.K., M.O.P., N.B., and S.C.D. Visualization: A.S., B.L., I.G., G.M., L.K.K., K.V., S.C.D., T.K., and T.P. Funding acquisition: A.N., S.S., T.K., T.P., U.K.K., and W.H. Project administration: T.K. Supervision: A.N., S.S., T.K., T.P., and U.K.K. Writing─original draft: B.L., S.S., T.K., and T.P. Writing─review and editing: A.N., A.S., GM, I.G., L.K.K., M.O.P., N.B., S.C.D., S.S., T.P., T.K., U.K.K., and W.H.

  • Notes
    The authors declare no competing financial interest.

    Data availability: Experimental data are available at https://doi.org/10.5281/zenodo.7382905. ResAM code is available at https://doi.org/10.5281/zenodo.7406941.

Acknowledgments

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This work was funded by the Swiss National Science Foundation (grant numbers 189939 and 196729). The authors thank Chuck Haas and Mutian Niu for valuable discussions and acknowledge Ramona Klein for the illustration of virus transmission.

References

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    Pandemic and seasonal influenza viruses can be transmitted through aerosols and droplets, in which viruses must remain stable and infectious across a wide range of environmental conditions. Using humidity-controlled chambers, we studied the impact of relative humidity on the stability of 2009 pandemic influenza A(H1N1) virus in suspended aerosols and stationary droplets. Contrary to the prevailing paradigm that humidity modulates the stability of respiratory viruses in aerosols, we found that viruses supplemented with material from the apical surface of differentiated primary human airway epithelial cells remained equally infectious for 1 h at all relative humidities tested. This sustained infectivity was obsd. in both fine aerosols and stationary droplets. Our data suggest, for the first time, that influenza viruses remain highly stable and infectious in aerosols across a wide range of relative humidities. These results have significant implications for understanding the mechanisms of transmission of influenza and its seasonality.
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    Brown, J. R.; Tang, J. W.; Pankhurst, L.; Klein, N.; Gant, V.; Lai, K. M.; McCauley, J.; Breuer, J. Influenza Virus Survival in Aerosols and Estimates of Viable Virus Loss Resulting from Aerosolization and Air-Sampling. J. Hosp. Infect. 2015, 91, 278– 281,  DOI: 10.1016/j.jhin.2015.08.004
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    Influenza virus survival in aerosols and estimates of viable virus loss resulting from aerosolization and air-sampling
    Brown J R; Tang J W; Pankhurst L; Klein N; Breuer J; Gant V; Lai K M; McCauley J
    The Journal of hospital infection (2015), 91 (3), 278-81 ISSN:.
    Using a Collison nebulizer, aerosols of influenza (A/Udorn/307/72 H3N2) were generated within a controlled experimental chamber, from known starting virus concentrations. Air samples collected after variable suspension times were tested quantitatively using both plaque and polymerase chain reaction assays, to compare the proportion of viable virus against the amount of detectable viral RNA. These experiments showed that whereas influenza RNA copies were well preserved, the number of viable viruses decreased by a factor of 10(4)-10(5). This suggests that air-sampling studies for assessing infection control risks that detect only influenza RNA may greatly overestimate the amount of viable virus available to cause infection.
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    Shechmeister, I. L. Studies on the Experimental Epidemiology of Respiratory Infections: III. Certain Aspects of the Behavior of Type A Influenza Virus as an Air-Borne Cloud. J. Infect. Dis. 1950, 87, 128– 132,  DOI: 10.1093/infdis/87.2.128
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    Studies on the experimental epidemiology of respiratory infections. III. Certain aspects of the behavior of type A influenza virus as an air-borne cloud
    SHECHMEISTER I L
    The Journal of infectious diseases (1950), 87 (2), 128-32 ISSN:0022-1899.
    There is no expanded citation for this reference.
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    Hemmes, J. H.; Winkler, K. C.; Kool, S. M. Virus Survival as a Seasonal Factor in Influenza and Poliomyelitis. Nature 1960, 188, 430– 431,  DOI: 10.1038/188430a0
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    Virus survival as a seasonal factor in influenza and polimyelitis
    HEMMES J H; WINKLER K C; KOOL S M
    Nature (1960), 188 (), 430-1 ISSN:0028-0836.
    There is no expanded citation for this reference.
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    Airborne micro-organisms: survival tests with four viruses
    HARPER G J
    The Journal of hygiene (1961), 59 (), 479-86 ISSN:0022-1724.
    There is no expanded citation for this reference.
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    Schaffer, F. L.; Soergel, M. E.; Straube, D. C. Survival of Airborne Influenza Virus: Effects of Propagating Host, Relative Humidity, and Composition of Spray Fluids. Arch. Virol. 1976, 51, 263– 273,  DOI: 10.1007/BF01317930
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    Survival of airborne influenza virus: effects of propagating host, relative humidity, and composition of spray fluids
    Schaffer, F. L.; Soergel, M. E.; Straube, D. C.
    Archives of Virology (1976), 51 (4), 263-73CODEN: ARVIDF; ISSN:0304-8608.
    Influenza A virus, strain WSNH, propagated in bovine, human, and chick embryo cell cultures and aerosolized from the cell culture medium, was maximally stable at low relative humidity (RH), minimally stable at mid-range RH, and moderately stable at high RH. Most lots of WSNH virus propagated in embryonated eggs and aerosolized from the allantoic fluid were also least stable at mid-range RH, but 2 prepns. after multiple serial passage in eggs showed equal stability at mid-range and higher RHs. Airborne stability varied from prepn. to prepn. of virus progated both in cell culture and embryonated eggs. There was no apparent correlation between airborne stability and protein content of spray fluid >0.1 mg/ml, but 1 prepn. of lesser protein concn. was extremely unstable at 50-80% RH. Polyhydroxy compds. exerted a protective effect on airborne stability.
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    Schuit, M.; Gardner, S.; Wood, S.; Bower, K.; Williams, G.; Freeburger, D.; Dabisch, P. The Influence of Simulated Sunlight on the Inactivation of Influenza Virus in Aerosols. J. Infect. Dis. 2020, 221, 372– 378,  DOI: 10.1093/infdis/jiz582
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    The Influence of Simulated Sunlight on the Inactivation of Influenza Virus in Aerosols
    Schuit Michael; Gardner Sierra; Wood Stewart; Bower Kristin; Williams Greg; Freeburger Denise; Dabisch Paul
    The Journal of infectious diseases (2020), 221 (3), 372-378 ISSN:.
    BACKGROUND: Environmental parameters, including sunlight levels, are known to affect the survival of many microorganisms in aerosols. However, the impact of sunlight on the survival of influenza virus in aerosols has not been previously quantified. METHODS: The present study examined the influence of simulated sunlight on the survival of influenza virus in aerosols at both 20% and 70% relative humidity using an environmentally controlled rotating drum aerosol chamber. RESULTS: Measured decay rates were dependent on the level of simulated sunlight, but they were not significantly different between the 2 relative humidity levels tested. In darkness, the average decay constant was 0.02 ± 0.06 min-1, equivalent to a half-life of 31.6 minutes. However, at full intensity simulated sunlight, the mean decay constant was 0.29 ± 0.09 min-1, equivalent to a half-life of approximately 2.4 minutes. CONCLUSIONS: These results are consistent with epidemiological findings that sunlight levels are inversely correlated with influenza transmission, and they can be used to better understand the potential for the virus to spread under varied environmental conditions.
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  12. 12
    Schuit, M.; Ratnesar-Shumate, S.; Yolitz, J.; Williams, G.; Weaver, W.; Green, B.; Miller, D.; Krause, M.; Beck, K.; Wood, S.; Holland, B.; Bohannon, J.; Freeburger, D.; Hooper, I.; Biryukov, J.; Altamura, L. A.; Wahl, V.; Hevey, M.; Dabisch, P. Airborne SARS-CoV-2 Is Rapidly Inactivated by Simulated Sunlight. J. Infect. Dis. 2020, 222, 564– 571,  DOI: 10.1093/infdis/jiaa334
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    Airborne SARS-CoV-2 is rapidly inactivated by simulated sunlight
    Schuit, Michael; Ratnesar-Shumate, Shanna; Yolitz, Jason; Williams, Gregory; Weaver, Wade; Green, Brian; Miller, David; Krause, Melissa; Beck, Katie; Wood, Stewart; Holland, Brian; Bohannon, Jordan; Freeburger, Denise; Hooper, Idris; Biryukov, Jennifer; Altamura, Louis A.; Wahl, Victoria; Hevey, Michael; Dabisch, Paul
    Journal of Infectious Diseases (2020), 222 (4), 564-571CODEN: JIDIAQ; ISSN:1537-6613. (Oxford University Press)
    Aerosols represent a potential transmission route of COVID-19. This study examd. effect of simulated sunlight, relative humidity, and suspension matrix on stability of SARS-CoV-2 in aerosols. Simulated sunlight and matrix significantly affected decay rate of the virus. Relative humidity alone did not affect the decay rate; however, minor interactions between relative humidity and other factors were obsd. Mean decay rates (± SD) in simulated saliva, under simulated sunlight levels representative of late winter/early fall and summer were 0.121 ± 0.017 min-1 (90% loss, 19 min) and 0.306 ± 0.097 min-1 (90% loss, 8 min), resp. Mean decay rate without simulated sunlight across all relative humidity levels was 0.008 ± 0.011 min-1 (90% loss, 286 min). These results suggest that the potential for aerosol transmission of SARS-CoV-2 may be dependent on environmental conditions, particularly sunlight. These data may be useful to inform mitigation strategies to minimize the potential for aerosol transmission.
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    Dabisch, P.; Schuit, M.; Herzog, A.; Beck, K.; Wood, S.; Krause, M.; Miller, D.; Weaver, W.; Freeburger, D.; Hooper, I.; Green, B.; Williams, G.; Holland, B.; Bohannon, J.; Wahl, V.; Yolitz, J.; Hevey, M.; Ratnesar-Shumate, S. The Influence of Temperature, Humidity, and Simulated Sunlight on the Infectivity of SARS-CoV-2 in Aerosols. Aerosol Sci. Technol. 2020, 55, 142,  DOI: 10.1080/02786826.2020.1829536
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    van Doremalen, N.; Bushmaker, T.; Morris, D. H.; Holbrook, M. G.; Gamble, A.; Williamson, B. N.; Tamin, A.; Harcourt, J. L.; Thornburg, N. J.; Gerber, S. I.; Lloyd-Smith, J. O.; de Wit, E.; Munster, V. J. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N. Engl. J. Med. 2020, 382, 1564– 1567,  DOI: 10.1056/NEJMc2004973
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    Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1
    van Doremalen Neeltje; Bushmaker Trenton; Holbrook Myndi G; Williamson Brandi N; de Wit Emmie; Munster Vincent J; Morris Dylan H; Gamble Amandine; Tamin Azaibi; Harcourt Jennifer L; Thornburg Natalie J; Gerber Susan I; Lloyd-Smith James O
    The New England journal of medicine (2020), 382 (16), 1564-1567 ISSN:.
    There is no expanded citation for this reference.
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    Ijaz, M. K.; Brunner, A. H.; Sattar, S. A.; Nair, R. C.; Johnson-Lussenburg, C. M. Survival Characteristics of Airborne Human Coronavirus 229E. J. Gen. Virol. 1985, 66, 2743– 2748,  DOI: 10.1099/0022-1317-66-12-2743
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    Survival characteristics of airborne human coronavirus 229E
    Ijaz M K; Brunner A H; Sattar S A; Nair R C; Johnson-Lussenburg C M
    The Journal of general virology (1985), 66 ( Pt 12) (), 2743-8 ISSN:0022-1317.
    The survival of airborne human coronavirus 229E (HCV/229E) was studied under different conditions of temperature (20 +/- 1 degree C and 6 +/- 1 degree C) and low (30 +/- 5%), medium (50 +/- 5%) or high (80 +/- 5%) relative humidities (RH). At 20 +/- 1 degree C, aerosolized HCV/229E was found to survive best at 50% RH with a half-life of 67.33 +/- 8.24 h while at 30% RH the virus half-life was 26.76 +/- 6.21 h. At 50% RH nearly 20% infectious virus was still detectable at 6 days. High RH at 20 +/- 1 degree C, on the other hand, was found to be the least favourable to the survival of aerosolized virus and under these conditions the virus half-life was only about 3 h; no virus could be detected after 24 h in aerosol. At 6 +/- 1 degree C, in either 50% or 30% RH conditions, the survival of HCV/229E was significantly enhanced, with the decay pattern essentially similar to that seen at 20 +/- 1 degree C. At low temperature and high RH (80%), however, the survival pattern was completely reversed, with the HCV/229E half-life increasing to 86.01 +/- 5.28 h, nearly 30 times that found at 20 +/- 1 degree C and high RH. Although optimal survival at 6 degree C still occurred at 50% RH, the pronounced stabilizing effect of low temperature on the survival of HCV/229E at high RH indicates that the role of the environment on the survival of viruses in air may be more complex and significant than previously thought.
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    Marr, L. C.; Tang, J. W.; Van Mullekom, J.; Lakdawala, S. S. Mechanistic Insights into the Effect of Humidity on Airborne Influenza Virus Survival, Transmission and Incidence. J. R. Soc., Interface 2019, 16, 20180298,  DOI: 10.1098/rsif.2018.0298
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    Mechanistic insights into the effect of humidity on airborne influenza virus survival, transmission and incidence
    Marr, Linsey C.; Tang, Julian W.; Van Mullekom, Jennifer; Lakdawala, Seema S.
    Journal of the Royal Society, Interface (2019), 16 (150), 20180298CODEN: JRSICU; ISSN:1742-5662. (Royal Society)
    A review. Influenza incidence and seasonality, along with virus survival and transmission, appear to depend at least partly on humidity, and recent studies have suggested that abs. humidity (AH) is more important than relative humidity (RH) in modulating obsd. patterns. In this perspective article, we re-evaluate studies of influenza virus survival in aerosols, transmission in animal models and influenza incidence to show that the combination of temp. and RH is equally valid as AH as a predictor. Collinearity must be considered, as higher levels of AH are only possible at higher temps., where it is well established that virus decay is more rapid. In studies of incidence that employ meteorol. data, outdoor AH may be serving as a proxy for indoor RH in temperate regions during the wintertime heating season. Finally, we present a mechanistic explanation based on droplet evapn. and its impact on droplet physics and chem. for why RH is more likely than AH to modulate virus survival and transmission.
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    Lin, K.; Marr, L. C. Humidity-Dependent Decay of Viruses, but Not Bacteria, in Aerosols and Droplets Follows Disinfection Kinetics. Environ. Sci. Technol. 2020, 54, 1024– 1032,  DOI: 10.1021/acs.est.9b04959
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    17
    Humidity-Dependent Decay of Viruses, but Not Bacteria, in Aerosols and Droplets Follows Disinfection Kinetics
    Lin, Kaisen; Marr, Linsey C.
    Environmental Science & Technology (2020), 54 (2), 1024-1032CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
    The transmission of some infectious diseases requires that pathogens can survive (i.e., remain infectious) in the environment, outside the host. Relative humidity (RH) is known to affect the survival of some microorganisms in the environment; however, the mechanism underlying the relationship has not been explained, particularly for viruses. We investigated the effects of RH on the viability of bacteria and viruses in both suspended aerosols and stationary droplets using traditional culture-based approaches. Results showed that viability of bacteria generally decreased with decreasing RH. Viruses survived well at RHs lower than 33% and at 100%, whereas their viability was reduced at intermediate RHs. We then explored the evapn. rate of droplets consisting of culture media and the resulting changes in solute concns. over time; as water evaps. from the droplets, solutes such as sodium chloride in the media become more concd. Based on the results, we suggest that inactivation of bacteria is influenced by osmotic pressure resulting from elevated concns. of salts as droplets evap. We propose that the inactivation of viruses is governed by the cumulative dose of solutes or the product of concn. and time, as in disinfection kinetics. These findings emphasize that evapn. kinetics play a role in modulating the survival of microorganisms in droplets.
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  18. 18
    Morris, D. H.; Yinda, K. C.; Gamble, A.; Rossine, F. W.; Huang, Q.; Bushmaker, T.; Fischer, R. J.; Matson, M. J.; Van Doremalen, N.; Vikesland, P. J.; Marr, L. C.; Munster, V. J.; Lloyd-Smith, J. O. Mechanistic Theory Predicts the Effects of Temperature and Humidity on Inactivation of SARS-CoV-2 and Other Enveloped Viruses. eLife 2021, 10, e65902  DOI: 10.7554/eLife.65902
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    18
    Mechanistic theory predicts the effects of temperature and humidity on inactivation of SARS-CoV-2 and other enveloped viruses
    Morris, Dylan H.; Yinda, Kwe Claude; Gamble, Amandine; Rossine, Fernando W.; Huang, Qishen; Bushmaker, Trenton; Fischer, Robert J.; Matson, M. Jeremiah; Van Doremalen, Neeltje; Vikesland, Peter J.; Marr, Linsey C.; Munster, Vincent J.; Lloyd-Smith, James O.
    eLife (2021), 10 (), e65902CODEN: ELIFA8; ISSN:2050-084X. (eLife Sciences Publications Ltd.)
    Ambient temp. and humidity strongly affect inactivation rates of enveloped viruses, but a mechanistic, quant. theory of these effects has been elusive. We measure the stability of SARS-CoV-2 on an inert surface at nine temp. and humidity conditions and develop a mechanistic model to explain and predict how temp. and humidity alter virus inactivation. We fiend SARS-CoV-2 survives longest at low temps. and extreme relative humidities (RH); median estd. virus half-life is >24 h at 10°C and 40% RH, but -1.5 h at 27°C and 65% RH. Our mechanistic model uses fundamental chem. to explain why inactivation rate increases with increased temp. and shows a U-shaped dependence on RH. The model accurately predicts existing measurements of five different human coronaviruses, suggesting that shared mechanisms may affect stability for many viruses. The results indicate scenarios of high transmission risk, point to mitigation strategies, and advance the mechanistic study of virus transmission.
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    Niazi, S.; Groth, R.; Cravigan, L.; He, C.; Tang, J. W.; Spann, K.; Johnson, G. R. Susceptibility of an Airborne Common Cold Virus to Relative Humidity. Environ. Sci. Technol. 2021, 55, 499– 508,  DOI: 10.1021/acs.est.0c06197
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    19
    Susceptibility of an Airborne Common Cold Virus to Relative Humidity
    Niazi, Sadegh; Groth, Robert; Cravigan, Luke; He, Congrong; Tang, Julian W.; Spann, Kirsten; Johnson, Graham R.
    Environmental Science & Technology (2021), 55 (1), 499-508CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
    The viability of airborne respiratory viruses varies with ambient relative humidity (RH). Numerous contrasting reports spanning several viruses have failed to identify the mechanism underlying this dependence. We hypothesized that an "efflorescence/deliquescence divergent infectivity" (EDDI) model accurately predicts the RH-dependent survival of airborne human rhinovirus-16 (HRV-16). We measured the efflorescence and deliquescence RH (RHE and RHD, resp.) of aerosols nebulized from a protein-enriched saline carrier fluid simulating the human respiratory fluid and found the RH range of the aerosols' hygroscopic hysteresis zone (RHE-D) to be 38-68%, which encompasses the preferred RH for indoor air (40-60%). The carrier fluid contg. HRV-16 was nebulized into the sub-hysteresis zone (RH<E) or super-hysteresis zone (RH>D) air, to set the aerosols to the effloresced/solid or deliquesced/liq. state before transitioning the RH into the intermediate hysteresis zone. The surviving fractions (SFs) of the virus were then measured 15 min post nebulization. SFs were also measured for aerosols introduced directly into the RH<E, RHE-D, and RH>D zones without transition. SFs for transitioned aerosols in the hysteresis zone were higher for effloresced (0.17 ± 0.02) than for deliquesced (0.005 ± 0.005) aerosols. SFs for nontransitioned aerosols in the RH<E, RHE-D, and RH>D zones were 0.18 ± 0.06, 0.05 ± 0.02, and 0.20 ± 0.05, resp., revealing a V-shaped SF/RH dependence. The EDDI model's prediction of enhanced survival in the hysteresis zone for effloresced carrier aerosols was confirmed.
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  20. 20
    Niazi, S.; Short, K. R.; Groth, R.; Cravigan, L.; Spann, K.; Ristovski, Z.; Johnson, G. R. Humidity-Dependent Survival of an Airborne Influenza A Virus: Practical Implications for Controlling Airborne Viruses. Environ. Sci. Technol. Lett. 2021, 8, 412– 418,  DOI: 10.1021/acs.estlett.1c00253
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    20
    Humidity-Dependent Survival of an Airborne Influenza A Virus: Practical Implications for Controlling Airborne Viruses
    Niazi, Sadegh; Short, Kirsty R.; Groth, Robert; Cravigan, Luke; Spann, Kirsten; Ristovski, Zoran; Johnson, Graham R.
    Environmental Science & Technology Letters (2021), 8 (5), 412-418CODEN: ESTLCU; ISSN:2328-8930. (American Chemical Society)
    Relative humidity (RH) can affect influenza A virus (IAV) survival. However, the mechanism driving this relationship is unknown. We hypothesized that the RH-dependent survival of airborne IAV could be predicted by the efflorescence/deliquescence divergent infectivity (EDDI) hypothesis. We detd. three distinct RH response zones based on the hygroscopic growth factor of carrier aerosols. These zones were classified as the super-deliquescence zone (RH > 75%), the hysteresis zone (43% < RH < 75%), and the sub-efflorescence zone (RH < 43%). We added IAV (H3N2) to protein-enriched saline and aerosolized it into sub-efflorescence or super-deliquescence zone air, yielding aerosols in the effloresced or noneffloresced state, resp. We then adjusted the RH to an ergonomically comfortable RH (60%). Fifteen minutes post-aerosolization, the surviving fractions (arithmetic means ± std. errors) of virus were higher in effloresced aerosols (9.5 ± 0.5%) than in non-effloresced aerosols (0.40 ± 0.05%). A virus suspension was also aerosolized directly into air within the super-deliquescence, hysteresis, and sub-efflorescence zones to assess the impact of the sudden change in RH from an initial 100% satd. RH to these zonal ranges. Fifteen minutes post-aerosolization, the surviving fractions were 3 ± 0.4%, 2 ± 0.1%, and 12 ± 2%, resp. Survival following gradual adaptation to the hysteresis zone RH range was sustained in effloresced and reduced in the non-effloresced aerosols. The EDDI model predicted the survival of IAV under seasonal conditions, offering strategies for controlling indoor air infection.
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    Yang, W.; Elankumaran, S.; Marr, L. C. Relationship between Humidity and Influenza A Viability in Droplets and Implications for Influenza’s Seasonality. PloS One 2012, 7, e46789  DOI: 10.1371/journal.pone.0046789
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    Relationship between humidity and influenza a viability in droplets and implications for influenza's seasonality
    Yang, Wan; Elankumaran, Subbiah; Marr, Linsey C.
    PLoS One (2012), 7 (10), e46789CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
    Humidity has been assocd. with influenza's seasonality, but the mechanisms underlying the relationship remain unclear. There is no consistent explanation for influenza's transmission patterns that applies to both temperate and tropical regions. This study aimed to det. the relationship between ambient humidity and viability of the influenza A virus (IAV) during transmission between hosts and to explain the mechanisms underlying it. We measured the viability of IAV in droplets consisting of various model media, chosen to isolate effects of salts and proteins found in respiratory fluid, and in human mucus, at relative humidities (RH) ranging from 17% to 100%. In all media and mucus, viability was highest when RH was either close to 100% or below ∼50%. When RH decreased from 84% to 50%, the relationship between viability and RH depended on droplet compn.: viability decreased in saline solns., did not change significantly in solns. supplemented with proteins, and increased dramatically in mucus. Addnl., viral decay increased linearly with salt concn. in saline solns. but not when they were supplemented with proteins. There appear to be three regimes of IAV viability in droplets, defined by humidity: physiol. conditions (∼100% RH) with high viability, concd. conditions (50% to near 100% RH) with lower viability depending on the compn. of media, and dry conditions (<50% RH) with high viability. This paradigm could help resolve conflicting findings in the literature on the relationship between IAV viability in aerosols and humidity, and results in human mucus could help explain influenza's seasonality in different regions.
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    Weber, R. J.; Guo, H.; Russell, A. G.; Nenes, A. High Aerosol Acidity despite Declining Atmospheric Sulfate Concentrations over the Past 15 Years. Nat. Geosci. 2016, 9, 282– 285,  DOI: 10.1038/ngeo2665
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    High aerosol acidity despite declining atmospheric sulfate concentrations over the past 15 years
    Weber, Rodney J.; Guo, Hongyu; Russell, Armistead G.; Nenes, Athanasios
    Nature Geoscience (2016), 9 (4), 282-285CODEN: NGAEBU; ISSN:1752-0894. (Nature Publishing Group)
    Particle acidity affects aerosol concns., chem. compn. and toxicity. Sulfate is often the main acid component of aerosols, and largely dets. the acidity of fine particles under 2.5 μm in diam., PM2.5. Over the past 15 years, atm. sulfate concns. in the southeastern United States have decreased by 70%, whereas ammonia concns. have been steady. Similar trends are occurring in many regions globally. Aerosol ammonium nitrate concns. were assumed to increase to compensate for decreasing sulfate, which would result from increasing neutrality. Here we use obsd. gas and aerosol compn., humidity, and temp. data collected at a rural southeastern US site in June and July 2013 (ref. 1), and a thermodn. model that predicts pH and the gas-particle equil. concns. of inorg. species from the observations to show that PM2.5 at the site is acidic. PH buffering by partitioning of ammonia between the gas and particle phases produced a relatively const. particle pH of 0-2 throughout the 15 years of decreasing atm. sulfate concns., and little change in particle ammonium nitrate concns. We conclude that the redns. in aerosol acidity widely anticipated from sulfur redns., and expected acidity-related health and climate benefits, are unlikely to occur until atm. sulfate concns. reach near pre-anthropogenic levels.
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    Scholtissek, C. Stability of Infectious Influenza A Viruses to Treatment at Low PH and Heating. Arch. Virol. 1985, 85, 1– 11,  DOI: 10.1007/BF01317001
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    Stability of infectious influenza A viruses to treatment at low pH and heating
    Scholtissek C
    Archives of virology (1985), 85 (1-2), 1-11 ISSN:0304-8608.
    We have measured the infectivity of influenza A virus strains grown either in embryonated eggs or in chick embryo cells in culture after treatment at low pH. At pH values at which hemolysis occurs there was an irreversible loss of infectivity. The threshold pH, at which the infectivity was lost, depended on the hemagglutinin subtype of the virus strain. All H5 and H7 strains tested were extremely labile at low pH. In contrast, all H3 strains were relatively stable, independent of the species from which the viruses were isolated. With several H1 viruses the hemagglutination (HA) activity was irreversibly lost at intermediate pH values causing inactivation of infectivity. Strains with noncleaved hemagglutinins were much more stable. These observations might explain why duck influenza viruses can easily survive in lake water and wet faeces, and multiply in the intestinal tract, where trypsin is present. There are also significant differences in heat stability exhibited by influenza A strains. In contrast to pH stability this is not a specific trait of the hemagglutinin, since it can be influenced by reassortment. There is no correlation between the stability of infectivity at low pH and heat.
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    Yang, W.; Marr, L. C. Mechanisms by Which Ambient Humidity May Affect Viruses in Aerosols. Appl. Environ. Microbiol. 2012, 78, 6781– 6788,  DOI: 10.1128/AEM.01658-12
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    Mechanisms by which ambient humidity may affect viruses in aerosols
    Yang, Wan; Marr, Linsey C.
    Applied and Environmental Microbiology (2012), 78 (19), 6781-6788CODEN: AEMIDF; ISSN:0099-2240. (American Society for Microbiology)
    A review. Many airborne viruses have been shown to be sensitive to ambient humidity, yet the mechanisms responsible for this phenomenon remain elusive. We review multiple hypotheses, including water activity, surface inactivation, and salt toxicity, that may account for the assocn. between humidity and viability of viruses in aerosols. We assess the evidence and limitations for each hypothesis based on findings from virol., aerosol science, chem., and physics. In addn., we hypothesize that changes in pH within the aerosol that are induced by evapn. may trigger conformational changes of the surface glycoproteins of enveloped viruses and subsequently compromise their infectivity. This hypothesis may explain the differing responses of enveloped viruses to humidity. The precise mechanisms underlying the relationship remain largely unverified, and attaining a complete understanding of them will require an interdisciplinary approach.
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    Pye, H. O. T.; Nenes, A.; Alexander, B.; Ault, A. P.; Barth, M. C.; Clegg, S. L.; Collett, J. L., Jr.; Fahey, K. M.; Hennigan, C. J.; Herrmann, H.; Kanakidou, M.; Kelly, J. T.; Ku, I.-T.; McNeill, V. F.; Riemer, N.; Schaefer, T.; Shi, G.; Tilgner, A.; Walker, J. T.; Wang, T.; Weber, R.; Xing, J.; Zaveri, R. A.; Zuend, A. The Acidity of Atmospheric Particles and Clouds. Atmos. Chem. Phys. 2020, 20, 4809– 4888,  DOI: 10.5194/acp-20-4809-2020
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    The acidity of atmospheric particles and clouds
    Pye, Havala O. T.; Nenes, Athanasios; Alexander, Becky; Ault, Andrew P.; Barth, Mary C.; Clegg, Simon L.; Collett, Jeffrey L., Jr.; Fahey, Kathleen M.; Hennigan, Christopher J.; Herrmann, Hartmut; Kanakidou, Maria; Kelly, James T.; Ku, I-Ting; McNeill, V. Faye; Riemer, Nicole; Schaefer, Thomas; Shi, Guoliang; Tilgner, Andreas; Walker, John T.; Wang, Tao; Weber, Rodney; Xing, Jia; Zaveri, Rahul A.; Zuend, Andreas
    Atmospheric Chemistry and Physics (2020), 20 (8), 4809-4888CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
    Acidity, defined as pH, is a central component of aq. chem. In the atm., the acidity of condensed phases (aerosol particles, cloud water, and fog droplets) governs the phase partitioning of semivolatile gases such as HNO3, NH3, HCl, and org. acids and bases as well as chem. reaction rates. It has implications for the atm. lifetime of pollutants, deposition, and human health. Despite its fundamental role in atm. processes, only recently has this field seen a growth in the no. of studies on particle acidity. Even with this growth, many fine-particle pH ests. must be based on thermodn. model calcns. since no operational techniques exist for direct measurements. Current information indicates acidic fine particles are ubiquitous, but observationally constrained pH ests. are limited in spatial and temporal coverage. Clouds and fogs are also generally acidic, but to a lesser degree than particles, and have a range of pH that is quite sensitive to anthropogenic emissions of sulfur and nitrogen oxides, as well as ambient ammonia. Historical measurements indicate that cloud and fog droplet pH has changed in recent decades in response to controls on anthropogenic emissions, while the limited trend data for aerosol particles indicate acidity may be relatively const. due to the semivolatile nature of the key acids and bases and buffering in particles. This paper reviews and synthesizes the current state of knowledge on the acidity of atm. condensed phases, specifically particles and cloud droplets. It includes recommendations for estg. acidity and pH, std. nomenclature, a synthesis of current pH ests. based on observations, and new model calcns. on the local and global scale.
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    Oswin, H. P.; Haddrell, A. E.; Otero-Fernandez, M.; Mann, J. F. S.; Cogan, T. A.; Hilditch, T. G.; Tian, J.; Hardy, D. A.; Hill, D. J.; Finn, A.; Davidson, A. D.; Reid, J. P. The Dynamics of SARS-CoV-2 Infectivity with Changes in Aerosol Microenvironment. Proc. Natl. Acad. Sci. U.S.A. 2022, 119, e2200109119  DOI: 10.1073/pnas.2200109119
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    Huang, Y. The SARS Epidemic and Its Aftermath in China: A Political Perspective. In Learning from SARS─Preparing for the Next Disease Outbreak: Workshop Summary; Institute of Medicine, The National Academies Press: Washington DC, 2004; pp 116– 136.
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    Nah, T.; Guo, H.; Sullivan, A. P.; Chen, Y.; Tanner, D. J.; Nenes, A.; Russell, A.; Ng, N.; Huey, L.; Weber, R. J. Characterization of Aerosol Composition, Aerosol Acidity, and Organic Acid Partitioning at an Agriculturally Intensive Rural Southeastern US Site. Atmos. Chem. Phys. 2018, 18, 11471– 11491,  DOI: 10.5194/acp-18-11471-2018
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    Characterization of aerosol composition, aerosol acidity, and organic acid partitioning at an agriculturally intensive rural southeastern US site
    Nah, Theodora; Guo, Hongyu; Sullivan, Amy P.; Chen, Yunle; Tanner, David J.; Nenes, Athanasios; Russell, Armistead; Ng, Nga Lee; Huey, L. Gregory; Weber, Rodney J.
    Atmospheric Chemistry and Physics (2018), 18 (15), 11471-11491CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
    The implementation of stringent emission regulations has resulted in the decline of anthropogenic pollutants including sulfur dioxide (SO2), nitrogen oxides (NOx), and carbon monoxide (CO). In contrast, ammonia (NH3) emissions are largely unregulated, with emissions projected to increase in the future. We present real-time aerosol and gas measurements from a field study conducted in an agriculturally intensive region in the southeastern US during the fall of 2016 to investigate how NH3 affects particle acidity and secondary org. aerosol (SOA) formation via the gas-particle partitioning of semi-volatile org. acids. Particle water and pH were detd. using the ISORROPIA II thermodn. model and validated by comparing predicted inorg. HNO3-NO3- and NH3-NHC4 gas-particle partitioning ratios with measured values. Our results showed that despite the high NH3 concns. (av. 8.1±5.2 ppb), PM1 was highly acidic with pH values ranging from 0.9 to 3.8, and an av. pH of 2.2±0.6. PM1 pH varied by approx. 1.4 units diurnally. Measured particle-phase water-sol. org. acids were on av. 6% of the total non-refractory PM1 org. aerosol mass. The measured oxalic acid gas-particle partitioning ratios were in good agreement with their corresponding thermodn. predictions, calcd. based on oxalic acid's physicochem. properties, ambient temp., particle water, and pH.
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    Brauer, M.; Koutrakis, P.; Keeler, G. J.; Spengler, J. D. Indoor and Outdoor Concentrations of Inorganic Acidic Aerosols and Gases. J. Air Waste Manage. Assoc. 1991, 41, 171– 181,  DOI: 10.1080/10473289.1991.10466834
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    Indoor and outdoor concentrations of inorganic acidic aerosols and gases
    Brauer, Michael; Koutrakis, Petros; Keeler, Gerald J.; Spengler, John D.
    Journal of the Air & Waste Management Association (1990-1992) (1991), 41 (2), 171-81CODEN: JAWAEB; ISSN:1047-3289.
    Annular denuder-filter pack sampling systems were used to make indoor and outdoor measurements of aerosol strong H+, SO42-, NH4+, NO3-, and NO2-, and the gaseous pollutants SO2, HNO3, HONO, and NH3 during summer and winter periods in Boston, Massachusetts. Outdoor levels of SO2, HNO3, H+, and SO42- exceeded their indoor concns. during both seasons. Winter indoor/outdoor ratios were lower than during the summer, probably due to lower air exchange rates during the winter period. During both monitoring periods, indoor/outdoor ratios of aerosol strong H+ were 40-50% of the indoor/outdoor SO42- ratio. Since aerosol strong acidity is typically assocd. with SO42-, this finding is indicative of neutralization of the acidic aerosol by the higher indoor NH3 levels. Geometric mean indoor/outdoor NH3 ratios of 3.5 and 23 resp. were measured for the summer and winter sampling periods. For HONO, NH3, NH4+, and NO2-, indoor concns. were significantly higher than ambient levels. Indoor levels of NO3- were slightly less than outdoor concns.
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    Nazaroff, W. W.; Weschler, C. J. Indoor Acids and Bases. Indoor Air 2020, 30, 559– 644,  DOI: 10.1111/ina.12670
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    Indoor acids and bases
    Nazaroff, William W.; Weschler, Charles J.
    Indoor Air (2020), 30 (4), 559-644CODEN: INAIE5; ISSN:1600-0668. (Wiley-Blackwell)
    A review. Numerous acids and bases influence indoor air quality. The most abundant of these species are CO2 (acidic) and NH3 (basic), both emitted by building occupants. Other prominent inorg. acids are HNO3, HONO, SO2, H2SO4, HCl, and HOCl. Prominent org. acids include formic, acetic, and lactic; nicotine is a noteworthy org. base. Sources of N-, S-, and Cl-contg. acids can include ventilation from outdoors, indoor combustion, consumer product use, and chem. reactions. Org. acids are commonly more abundant indoors than outdoors, with indoor sources including occupants, wood, and cooking. Beyond NH3 and nicotine, other noteworthy bases include inorg. and org. amines. Acids and bases partition indoors among the gas-phase, airborne particles, bulk water, and surfaces; relevant thermodn. parameters governing the partitioning are the acid-dissocn. const. (Ka), Henry's law const. (KH), and the octanol-air partition coeff. (Koa). Condensed-phase water strongly influences the fate of indoor acids and bases and is also a medium for chem. interactions. Indoor surfaces can be large reservoirs of acids and bases. This extensive review of the state of knowledge establishes a foundation for future inquiry to better understand how acids and bases influence the suitability of indoor environments for occupants, cultural artifacts, and sensitive equipment.
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    Ampollini, L.; Katz, E. F.; Bourne, S.; Tian, Y.; Novoselac, A.; Goldstein, A. H.; Lucic, G.; Waring, M. S.; DeCarlo, P. F. Observations and Contributions of Real-Time Indoor Ammonia Concentrations during HOMEChem. Environ. Sci. Technol. 2019, 53, 8591– 8598,  DOI: 10.1021/acs.est.9b02157
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    Observations and Contributions of Real-Time Indoor Ammonia Concentrations during HOMEChem
    Ampollini, Laura; Katz, Erin F.; Bourne, Stephen; Tian, Yilin; Novoselac, Atila; Goldstein, Allen H.; Lucic, Gregor; Waring, Michael S.; DeCarlo, Peter F.
    Environmental Science & Technology (2019), 53 (15), 8591-8598CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
    Although NH3 usually occurs outdoors at 1-5 ppb concns., indoor NH3 concns. can be much higher. Indoor NH3 is strongly emitted by cleaning products, tobacco smoke, building materials, and humans. Due to its high reactivity, water soly., and tendency to sorb to surfaces, NH2 os difficult to measure; hence, a comprehensive evaluation of indoor NH3 concns. is under-studied. During HOMEChem, a comprehensive indoor chem. study in a test house in June 2018, real-time indoor NH3 concns. were measured using cavity ring-down spectroscopy. A mean unoccupied background concn. of 32 ppb was obsd.; NH3 concns. were enhanced by cooking, cleaning, and occupancy, reaching max. concns. of 130, 1592, and 99 ppb, resp. NH3 concns. were strongly affected by indoor temp. and HVAC (heating, ventilation, air conditioning) operations. In the absence of activity-based sources, HVAC operation was the main indoor NH3 concn. modulator.
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    Vaughan, J.; Ngamtrakulpanit, L.; Pajewski, T. N.; Turner, R.; Nguyen, T. A.; Smith, A.; Urban, P.; Hom, S.; Gaston, B.; Hunt, J. Exhaled Breath Condensate PH Is a Robust and Reproducible Assay of Airway Acidity. Eur. Respir. J. 2003, 22, 889– 894,  DOI: 10.1183/09031936.03.00038803
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    Exhaled breath condensate pH is a robust and reproducible assay of airway acidity
    Vaughan J; Ngamtrakulpanit L; Pajewski T N; Turner R; Nguyen T A; Smith A; Urban P; Hom S; Gaston B; Hunt J
    The European respiratory journal (2003), 22 (6), 889-94 ISSN:0903-1936.
    Exhaled breath condensate (EBC) pH is low in several lung diseases and it normalises with therapy. The current study examined factors relevant to EBC pH monitoring. Intraday and intraweek variability were studied in 76 subjects. The pH of EBC collected orally and from isolated lower airways was compared in an additional 32 subjects. Effects of ventilatory pattern (hyperventilation/hypoventilation), airway obstruction after methacholine, temperature (-44 to +13 degrees C) and duration of collection (2-7 min), and duration of sample storage (up to 2 yrs) were examined. All samples were collected with a disposable condensing device, and de-aerated with argon until pH measurement stabilised. Mean EBC pH (n=76 subjects, total samples=741) was 7.7+/-0.49 (mean+/-SD). Mean intraweek and intraday coefficients of variation were 4.5% and 3.5%. Control of EBC pH appears to be at the level of the lower airway. Temperature of collection, duration of collection and storage, acute airway obstruction, subject age, saliva pH, and profound hyperventilation and hypoventilation had no effect on EBC pH. The current authors conclude that in health, exhaled breath condensate pH is slightly alkaline, held in a narrow range, and is controlled by lower airway source fluid. Measurement of exhaled breath condensate pH is a simple, robust, reproducible and relevant marker of disease.
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    Colberg, C. A.; Krieger, U. K.; Peter, T. Morphological Investigations of Single Levitated H2SO4/NH3/H2O Aerosol Particles during Deliquescence/Efflorescence Experiments. J. Phys. Chem. A 2004, 108, 2700– 2709,  DOI: 10.1021/jp037628r
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    Morphological investigations of single levitated H2SO4/NH3/H2O aerosol particles during deliquescence/efflorescence experiments
    Colberg, Christina A.; Krieger, Ulrich K.; Peter, Thomas
    Journal of Physical Chemistry A (2004), 108 (14), 2700-2709CODEN: JPCAFH; ISSN:1089-5639. (American Chemical Society)
    In an electrodynamic particle trap, expts. with single levitated H2SO4/NH3/H2O aerosol particles have been performed under atm. conditions. Four anal. methods provide independent information on the aerosol compn. and structure (measurements of Mie scattering, Raman scattering, scattering fluctuations, and of mass). The morphol. of the aerosol particles and the water uptake and drying behavior are investigated including the detn. of deliquescence and efflorescence relative humidities. In general, the thermodn. data derived from the measurements are in good agreement with previous work. The obsd. solid phase is mostly letovicite [(NH4)3H(SO4)2] and sometimes ammonium sulfate [(NH4)2SO4], whereas ammonium bisulfate [(NH4)HSO4] does not nucleate at temps. between 260 and 270 K despite supersatn. over periods of up to 1 day. This underlines the atm. importance of letovicite, which has been ignored in most previous studies concg. on ammonium sulfate. When the stoichiometry of the aq. soln. in the droplets is chosen as neither that of ammonium sulfate nor letovicite, the particles forming after efflorescence are mixed-phase particles (solid/liq.), representing the usual case in the natural atm. Upon crystn. these mixed-phase particles reveal a range of different morphologies with a tendency to form complex cryst. structures with embedded liq. cavities, but there is no evidence for the occurrence of cryst. material surrounded by the remaining liq. This liq. possibly resides in grain boundaries or triple junctions between single crystals or in small pores and shows little mobility upon extensive drying, unless the shell-like surrounding solid cracks.
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    Steimer, S. S.; Krieger, U. K.; Te, Y. F.; Lienhard, D. M.; Huisman, A. J.; Luo, B. P.; Ammann, M.; Peter, T. Electrodynamic Balance Measurements of Thermodynamic, Kinetic, and Optical Aerosol Properties Inaccessible to Bulk Methods. Atmos. Meas. Tech. 2015, 8, 2397– 2408,  DOI: 10.5194/amt-8-2397-2015
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    Davis, E. J.; Buehler, M. F.; Ward, T. L. The double-ring electrodynamic balance for microparticle characterization. Rev. Sci. Instrum. 1990, 61, 1281– 1288,  DOI: 10.1063/1.1141227
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    The double-ring electrodynamic balance for microparticle characterization
    Davis, E. James; Buehler, Mark F.; Ward, Timothy L.
    Review of Scientific Instruments (1990), 61 (4), 1281-8CODEN: RSINAK; ISSN:0034-6748.
    A simple form of the electrodynamic balance, suitable for a wide range of microparticle measurements, is described and analyzed. The a.c. electrode of the device consists of a pair of parallel rings, and the dc endcaps are either simple disks or they can be eliminated entirely by applying suitable d.c. bias voltages to the rings. The stability characteristics of the device are detd. by extension of well-established stability theory, and expts. are compared with that theory. The device is particularly well-suited for detection of radioactive aerosols, for it has significant advantages over the bihyperboloidal device for radioactivity measurement. The detection of radioactivity levels of <20 pCi is feasible. Coupled with a Raman spectrometer, the balance serves as a stable "platform" for the study of the chem. of microparticles, and both qual. and quant. anal. of microdroplet chem. are demonstrated for binary droplets of 1-octadecene and 1-bromoctadecane.
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    Zobrist, B.; Soonsin, V.; Luo, B. P.; Krieger, U. K.; Marcolli, C.; Peter, T.; Koop, T. Ultra-Slow Water Diffusion in Aqueous Sucrose Glasses. Phys. Chem. Chem. Phys. 2011, 13, 3514,  DOI: 10.1039/c0cp01273d
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    Ultra-slow water diffusion in aqueous sucrose glasses
    Zobrist, Bernhard; Soonsin, Vacharaporn; Luo, Bei P.; Krieger, Ulrich K.; Marcolli, Claudia; Peter, Thomas; Koop, Thomas
    Physical Chemistry Chemical Physics (2011), 13 (8), 3514-3526CODEN: PPCPFQ; ISSN:1463-9076. (Royal Society of Chemistry)
    We present measurements of water uptake and release by single micrometer-sized aq. sucrose particles. The expts. were performed in an electrodynamic balance where the particles can be stored contact-free in a temp. and humidity controlled chamber for several days. Aq. sucrose particles react to a change in ambient humidity by absorbing/desorbing water from the gas phase. This water absorption (desorption) results in an increasing (decreasing) droplet size and a decreasing (increasing) solute concn. Optical techniques were employed to follow minute changes of the droplet's size, with a sensitivity of 0.2 nm, as a result of changes in temp. or humidity. We exposed several particles either to humidity cycles (between ∼2% and 90%) at 291 K or to const. relative humidity and temp. conditions over long periods of time (up to several days) at temps. ranging from 203 to 291 K. In doing so, a retarded water uptake and release at low relative humidities and/or low temps. was obsd. Under the conditions studied here, the kinetics of this water absorption/desorption process is controlled entirely by liq.-phase diffusion of water mols. Hence, it is possible to derive the translational diffusion coeff. of water mols., DH2O, from these data by simulating the growth or shrinkage of a particle with a liq.-phase diffusion model. Values for DH2O-values as low as 10-24 m2 s-1 are detd. using data at temps. down to 203 K deep in the glassy state. From the expt. and modeling we can infer strong concn. gradients within a single particle including a glassy skin in the outer shells of the particle. Such glassy skins practically isolate the liq. core of a particle from the surrounding gas phase, resulting in extremely long equilibration times for such particles, caused by the strongly non-linear relationship between concn. and DH2O. We present a new parameterization of DH2O that facilitates describing the stability of aq. food and pharmaceutical formulations in the glassy state, the processing of amorphous aerosol particles in spray-drying technol., and the suppression of heterogeneous chem. reactions in glassy atm. aerosol particles.
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    Tang, I. N.; Munkelwitz, H. R. Water Activities, Densities, and Refractive Indices of Aqueous Sulfates and Sodium Nitrate Droplets of Atmospheric Importance. J. Geophys. Res.: Atmos. 1994, 99, 18801– 18808,  DOI: 10.1029/94jd01345
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    Zardini, A. A.; Sjogren, S.; Marcolli, C.; Krieger, U. K.; Gysel, M.; Weingartner, E.; Baltensperger, U.; Peter, T. A Combined Particle Trap/HTDMA Hygroscopicity Study of Mixed Inorganic/Organic Aerosol Particles. Atmos. Chem. Phys. 2008, 8, 5589– 5601,  DOI: 10.5194/acp-8-5589-2008
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    A combined particle trap/HTDMA hygroscopicity study of mixed inorganic/organic aerosol particles
    Zardini, A. A.; Sjogren, S.; Marcolli, C.; Krieger, U. K.; Gysel, M.; Weingartner, E.; Baltensperger, U.; Peter, T.
    Atmospheric Chemistry and Physics (2008), 8 (18), 5589-5601CODEN: ACPTCE; ISSN:1680-7316. (Copernicus Publications)
    Atm. aerosols are often mixts. of inorg. and org. material. Orgs. can represent a large fraction of the total aerosol mass and are comprised of water-sol. and insol. compds. Increasing attention was paid in the last decade to the capability of mixed inorg./org. aerosol particles to take up water (hygroscopicity). We performed hygroscopicity measurements of internally mixed particles contg. ammonium sulfate and carboxylic acids (citric, glutaric, adipic acid) in parallel with an electrodynamic balance (EDB) and a hygroscopicity tandem differential mobility analyzer (HTDMA). The org. compds. were chosen to represent three distinct phys. states. During hygroscopicity cycles covering hydration and dehydration measured by the EDB and the HTDMA, pure citric acid remained always liq., adipic acid remained always solid, while glutaric acid could be either. We show that the hygroscopicity of mixts. of the above compds. is well described by the Zdanovskii-Stokes-Robinson (ZSR) relationship as long as the two-component particle is completely liq. in the ammonium sulfate/glutaric acid system; deviations up to 10% in mass growth factor (corresponding to deviations up to 3.5% in size growth factor) are obsd. for the ammonium sulfate/citric acid 1:1 mixt. at 80% RH. We observe even more significant discrepancies compared to what is expected from bulk thermodn. when a solid component is present. We explain this in terms of a complex morphol. resulting from the crystn. process leading to veins, pores, and grain boundaries which allow for water sorption in excess of bulk thermodn. predictions caused by the inverse Kelvin effect on concave surfaces.
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  39. 39
    Chýlek, P. Partial-Wave Resonances and the Ripple Structure in the Mie Normalized Extinction Cross Section. J. Opt. Soc. Am. 1976, 66, 285– 287,  DOI: 10.1364/JOSA.66.000285
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    Bastelberger, S.; Krieger, U. K.; Luo, B.; Peter, T. Diffusivity Measurements of Volatile Organics in Levitated Viscous Aerosol Particles. Atmos. Chem. Phys. 2017, 17, 8453– 8471,  DOI: 10.5194/acp-17-8453-2017
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    40
    Diffusivity measurements of volatile organics in levitated viscous aerosol particles
    Bastelberger, Sandra; Krieger, Ulrich K.; Luo, Beiping; Peter, Thomas
    Atmospheric Chemistry and Physics (2017), 17 (13), 8453-8471CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
    Field measurements indicating that atm. secondary org. aerosol (SOA) particles can be present in a highly viscous, glassy state have spurred numerous studies addressing low diffusivities of water in glassy aerosols. The focus of these studies is on kinetic limitations of hygroscopic growth and the plasticizing effect of water. In contrast, much less is known about diffusion limitations of org. mols. and oxidants in viscous matrixes. These may affect atm. chem. and gas-particle partitioning of complex mixts. with constituents of different volatility. In this study, we quantify the diffusivity of a volatile org. in a viscous matrix. Evapn. of single particles generated from an aq. soln. of sucrose and small amts. of volatile tetraethylene glycol (PEG-4) is investigated in an electrodynamic balance at controlled relative humidity (RH) and temp. The evaporative loss of PEG- 4 as detd. by Mie resonance spectroscopy is used in conjunction with a radially resolved diffusion model to retrieve translational diffusion coeffs. of PEG-4. Comparison of the exptl. derived diffusivities with viscosity ests. for the ternary system reveals a breakdown of the Stokes-Einstein relationship, which has often been invoked to infer diffusivity from viscosity. The evapn. of PEG-4 shows pronounced RH and temp. dependencies and is severely depressed for .ltorsim. 30 %, corresponding to diffusivities < 10-14 cm2 s-1 at temps. < 15 °C. The temp. dependence is strong, suggesting a diffusion activation energy of about 300 kJmol-1.We conclude that atm. volatile org. compds. can be subject to severe diffusion limitations in viscous org. aerosol particles. This may enable an important long-range transport mechanism for org. material, including pollutant mols. such as polycyclic arom. hydrocarbons (PAHs).
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  41. 41
    Dou, J.; Alpert, P. A.; Corral Arroyo, P.; Luo, B.; Schneider, F.; Xto, J.; Huthwelker, T.; Borca, C. N.; Henzler, K. D.; Raabe, J.; Watts, B.; Herrmann, H.; Peter, T.; Ammann, M.; Krieger, U. K. Photochemical Degradation of Iron(III) Citrate/Citric Acid Aerosol Quantified with the Combination of Three Complementary Experimental Techniques and a Kinetic Process Model. Atmos. Chem. Phys. 2021, 21, 315– 338,  DOI: 10.5194/acp-21-315-2021
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    41
    Photochemical degradation of iron(III) citrate/citric acid aerosol quantified with the combination of three complementary experimental techniques and a kinetic process model
    Dou, Jing; Alpert, Peter A.; Arroyo, Pablo Corral; Luo, Beiping; Schneider, Frederic; Xto, Jacinta; Huthwelker, Thomas; Borca, Camelia N.; Henzler, Katja D.; Raabe, Jorg; Watts, Benjamin; Herrmann, Hartmut; Peter, Thomas; Ammann, Markus; Krieger, Ulrich K.
    Atmospheric Chemistry and Physics (2021), 21 (1), 315-338CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
    Iron(III) carboxylate photochem. plays an important role in aerosol aging, esp. in the lower troposphere. These complexes can absorb light over a broad wavelength range, inducing the redn. of iron(III) and the oxidn. of carboxylate ligands. In the presence of O2, the ensuing radical chem. leads to further decarboxylation, and the prodn. of ·OH, HO·2, peroxides, and oxygenated volatile org. compds., contributing to particle mass loss. The ·OH, HO·2, and peroxides in turn reoxidize iron(II) back to iron(III), closing a photocatalytic cycle. This cycle is repeated, resulting in continual mass loss due to the release of CO2 and other volatile compds. In a cold and/or dry atm., org. aerosol particles tend to attain highly viscous states. While the impact of reduced mobility of aerosol constituents on dark chem. reactions has received substantial attention, studies on the effect of high viscosity on photochem. processes are scarce. Here, we choose iron(III) citrate (FeIII(Cit)) as a model light-absorbing iron carboxylate complex that induces citric acid (CA) degrdn. to investigate how transport limitations influence photochem. processes. Three complementary exptl. approaches were used to investigate kinetic transport limitations. The mass loss of single, levitated particles was measured with an electrodynamic balance, the oxidn. state of deposited particles was measured with X-ray spectromicroscopy, and HO·2 radical prodn. and release into the gas phase was obsd. in coated-wall flow-tube expts. We obsd. significant photochem. degrdn. with up to 80 ‰ mass loss within 24 h of light exposure. Interestingly, we also obsd. that mass loss always accelerated during irradn., resulting in an increase of the mass loss rate by about a factor of 10. When we increased relative humidity (RH), the obsd. particle mass loss rate also increased. This is consistent with strong kinetic transport limitations for highly viscous particles. To quant. compare these expts. and det. important phys. and chem. parameters, a numerical multilayered photochem. reaction and diffusion (PRAD) model was developed that treats chem. reactions and the transport of various species. The PRAD model was tuned to simultaneously reproduce all exptl. results as closely as possible and captured the essential chem. and transport during irradn. In particular, the photolysis rate of FeIII, the reoxidn. rate of FeII, HO·2 prodn., and the diffusivity of O2 in aq. FeIII(Cit) / CA system as function of RH and FeIII(Cit) / CA molar ratio could be constrained. This led to satisfactory agreement within model uncertainty for most but not all expts. performed. Photochem. degrdn. under atm. conditions predicted by the PRAD model shows that release of CO2 and repartitioning of org. compds. to the gas phase may be very important when attempting to accurately predict org. aerosol aging processes.
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    Carslaw, K. S.; Clegg, S. L.; Brimblecombe, P. A Thermodynamic Model of the System HCl-HNO3-H2SO4-H2O, Including Solubilities of HBr, from <200 to 328 K. J. Phys. Chem. 1995, 99, 11557– 11574,  DOI: 10.1021/j100029a039
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    42
    A Thermodynamic Model of the System HCl-HNO3-H2SO4-H2O, Including Solubilities of HBr, from <200 to 328 K
    Carslaw, Kenneth S.; Clegg, Simon L.; Brimblecombe, Peter
    Journal of Physical Chemistry (1995), 99 (29), 11557-74CODEN: JPCHAX; ISSN:0022-3654.
    A multicomponent mole-fraction-based thermodn. model, together with Henry's law consts. and the vapor pressure of pure water, was used to represent aq. phase activities, vapor pressures (of H2O, HNO3, HCl, and HBr), and satn. with respect to solid phases (ice, H2SO4·nH2O, HNO3·nH2O, and HCl·3H2O) in the system HCl-HBr-HNO3-H2SO4-H2O. The model is valid from 330 to <200 K, and up to ∼40 mol/kg total solute molality for solns. contg. mainly H2SO4 and HNO3. Model parameters for pure aq. H2SO4 were adopted from a previous study, and values for HNO3-H2O, HCl-H2O, and HBr-H2O were obtained by fitting to activity and osmotic coeffs., emf. (emf) measurements, vapor pressures, f. ps., and thermal (enthalpy and heat capacity) data. The model was tested by using measured partial pressures and solubilities of HCl in aq. H2SO4 from 330 to 200 K, HBr solubilities in aq. H2SO4 from ∼240 to 205 K, and HNO3 partial pressures and f. ps. for HNO3-H2SO4-H2O mixts. from 273.15 to <200 K. Ternary (mixt.) parameters were required only for HNO3-H2SO4-H2O. Solubilities of HNO3, HCl, and HBr in liq. stratospheric aerosols are calcd.
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    Luo, B.; Carslaw, K. S.; Peter, T.; Clegg, S. L. Vapour Pressures of H2SO4/HNO3/HCl/HBr/H2O Solutions to Low Stratospheric Temperatures. Geophys. Res. Lett. 1995, 22, 247– 250,  DOI: 10.1029/94GL02988
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    43
    Vapor pressures of H2SO4/HNO3/HCl/HBr/H2O solutions to low stratospheric temperatures
    Luo, Beiping; Carslaw, Kenneth S.; Peter, Thomas; Clegg, Simon L.
    Geophysical Research Letters (1995), 22 (3), 247-50CODEN: GPRLAJ; ISSN:0094-8276.
    Vapor pressures of H2O, HNO3, HCl and HBr over supercooled aq. mixts. with sulfuric acid have been calcd. using an activity coeff. model, for 185 K < T < 235 K, 0 < wt.% (H2SO4) + wt.%(HNO3) < 70, and assuming HCl and HBr to be minor constituents. Predicted vapor pressures agree well with most lab. data, and give confidence in the validity of the model. The results are parameterized as simple formulas, which reproduce the model results to within 40% and cover the entire stratospherically relevant range of compn. and temp.
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    Lin, K.; Schulte, C. R.; Marr, L. C. Survival of MS2 and Φ6 viruses in droplets as a function of relative humidity, pH, and salt, protein, and surfactant concentrations. PLoS One 2020, 15, e0243505  DOI: 10.1371/journal.pone.0243505
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    Survival of MS2 and Φ6 viruses in droplets as a function of relative humidity, pH, and salt, protein, and surfactant concentrations
    Lin, Kaisen; Schulte, Chase R.; Marr, Linsey C.
    PLoS One (2020), 15 (12), e0243505CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
    The survival of viruses in droplets is known to depend on droplets' chem. compn., which may vary in respiratory fluid between individuals and over the course of disease. This relationship is also important for understanding the persistence of viruses in droplets generated from wastewater, freshwater, and seawater. We investigated the effects of salt (0, 1, and 35 g/L), protein (0, 100, and 1000μg/mL), surfactant (0, 1, and 10μg/mL), and droplet pH (4.0, 7.0, and 10.0) on the viability of viruses in 1-μL droplets pipetted onto polystyrene surfaces and exposed to 20%, 50%, and 80% relative humidity (RH) using a culture-based approach. Results showed that viability of MS2, a non-enveloped virus, was generally higher than that of Φ6, an enveloped virus, in droplets after 1 h. The chem. compn. of droplets greatly influenced virus viability. Specifically, the survival of MS2 was similar in droplets at different pH values, but the viability of Φ6 was significantly reduced in acidic and basic droplets compared to neutral ones. The presence of bovine serum albumin protected both MS2 and Φ6 from inactivation in droplets. The effects of sodium chloride and the surfactant sodium dodecyl sulfate varied by virus type and RH. Meanwhile, RH affected the viability of viruses as shown previously: viability was lowest at intermediate to high RH. The results demonstrate that the viability of viruses is detd. by the chem. compn. of carrier droplets, esp. pH and protein content, and environmental factors. These findings emphasize the importance of understanding the chem. compn. of carrier droplets in order to predict the persistence of viruses contained in them.
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    Galloway, S. E.; Reed, M. L.; Russell, C. J.; Steinhauer, D. A. Influenza HA Subtypes Demonstrate Divergent Phenotypes for Cleavage Activation and PH of Fusion: Implications for Host Range and Adaptation. PLoS Pathog. 2013, 9, e1003151  DOI: 10.1371/journal.ppat.1003151
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    Influenza HA subtypes demonstrate divergent phenotypes for cleavage activation and pH of fusion: implications for host range and adaptation
    Galloway, Summer E.; Reed, Mark L.; Russell, Charles J.; Steinhauer, David A.
    PLoS Pathogens (2013), 9 (2), e1003151CODEN: PPLACN; ISSN:1553-7374. (Public Library of Science)
    The influenza A virus (IAV) HA protein must be activated by host cells proteases in order to prime the mol. for fusion. Consequently, the availability of activating proteases and the susceptibility of HA to protease activity represents key factors in facilitating virus infection. As such, understanding the intricacies of HA cleavage by various proteases is necessary to derive insights into the emergence of pandemic viruses. To examine these properties, we generated a panel of HAs that are representative of the 16 HA subtypes that circulate in aquatic birds, as well as HAs representative of the subtypes that have infected the human population over the last century. We examd. the susceptibility of the panel of HA proteins to trypsin, as well as human airway trypsin-like protease (HAT) and transmembrane protease, serine 2 (TMPRSS2). Addnl., we examd. the pH at which these HAs mediated membrane fusion, as this property is related to the stability of the HA mol. and influences the capacity of influenza viruses to remain infectious in natural environments. Our results show that cleavage efficiency can vary significantly for individual HAs, depending on the protease, and that some HA subtypes display stringent selectivity for specific proteases as activators of fusion function. Addnl., we found that the pH of fusion varies by 0.7 pH units among the subtypes, and notably, we obsd. that the pH of fusion for most HAs from human isolates was lower than that obsd. from avian isolates of the same subtype. Overall, these data provide the first broad-spectrum anal. of cleavage-activation and membrane fusion characteristics for all of the IAV HA subtypes, and also show that there are substantial differences between the subtypes that may influence transmission among hosts and establishment in new species.
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    Bullough, P. A.; Hughson, F. M.; Skehel, J. J.; Wiley, D. C. Structure of Influenza Haemagglutinin at the PH of Membrane Fusion. Nature 1994, 371, 37– 43,  DOI: 10.1038/371037a0
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    Structure of influenza hemagglutinin at the pH of membrane fusion
    Bullough, Per A.; Hughson, Frederick M.; Skehel, John J.; Wiley, Don C.
    Nature (London, United Kingdom) (1994), 371 (6492), 37-43CODEN: NATUAS; ISSN:0028-0836.
    Low pH induces a conformational change in the influenza virus hemagglutinin, which then mediates fusion of the viral and host cell membranes. The three-dimensional structure of a fragment of the hemagglutinin in this conformation reveals a major refolding of the secondary and tertiary structure of the mol. The apolar fusion peptide moves at least 100 Å to one tip of the mol. At the other end a helical segment unfolds, a subdomain relocates reversing the chain direction, and part of the structure becomes disordered.
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    Jackson, C. B.; Farzan, M.; Chen, B.; Choe, H. Mechanisms of SARS-CoV-2 Entry into Cells. Nat. Rev. Mol. Cell Biol. 2022, 23, 3– 20,  DOI: 10.1038/s41580-021-00418-x
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    Mechanisms of SARS-CoV-2 entry into cells
    Jackson, Cody B.; Farzan, Michael; Chen, Bing; Choe, Hyeryun
    Nature Reviews Molecular Cell Biology (2022), 23 (1), 3-20CODEN: NRMCBP; ISSN:1471-0072. (Nature Portfolio)
    A review. The unprecedented public health and economic impact of the COVID-19 pandemic caused by infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been met with an equally unprecedented scientific response. Much of this response has focused, appropriately, on the mechanisms of SARS-CoV-2 entry into host cells, and in particular the binding of the spike (S) protein to its receptor, angiotensin-converting enzyme 2 (ACE2), and subsequent membrane fusion. This Review provides the structural and cellular foundations for understanding the multistep SARS-CoV-2 entry process, including S protein synthesis, S protein structure, conformational transitions necessary for assocn. of the S protein with ACE2, engagement of the receptor-binding domain of the S protein with ACE2, proteolytic activation of the S protein, endocytosis and membrane fusion. We define the roles of furin-like proteases, transmembrane protease, serine 2 (TMPRSS2) and cathepsin L in these processes, and delineate the features of ACE2 orthologues in reservoir animal species and S protein adaptations that facilitate efficient human transmission. We also examine the utility of vaccines, antibodies and other potential therapeutics targeting SARS-CoV-2 entry mechanisms. Finally, we present key outstanding questions assocd. with this crit. process.
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    Huynh, E.; Olinger, A.; Woolley, D.; Kohli, R. K.; Choczynski, J. M.; Davies, J. F.; Lin, K.; Marr, L. C.; Davis, R. D. Evidence for a Semisolid Phase State of Aerosols and Droplets Relevant to the Airborne and Surface Survival of Pathogens. Proc. Natl. Acad. Sci. U.S.A. 2022, 119, e2109750119  DOI: 10.1073/pnas.2109750119
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    Evidence for a semisolid phase state of aerosols and droplets relevant to the airborne and surface survival of pathogens
    Huynh, Erik; Olinger, Anna; Woolley, David; Kohli, Ravleen Kaur; Choczynski, Jack M.; Davies, James F.; Lin, Kaisen; Marr, Linsey C.; Davis, Ryan D.
    Proceedings of the National Academy of Sciences of the United States of America (2022), 119 (4), e2109750119CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
    The phase state of respiratory aerosols and droplets has been linked to the humidity-dependent survival of pathogens such as SARS-CoV-2. To inform strategies to mitigate the spread of infectious disease, it is thus necessary to understand the humidity-dependent phase changes assocd. with the particles in which pathogens are suspended. Here, we study phase changes of levitated aerosols and droplets composed of model respiratory compds. (salt and protein) and growth media (org.-inorg. mixts. commonly used in studies of pathogen survival) with decreasing relative humidity (RH). Efflorescence was suppressed in many particle compns. and thus unlikely to fully account for the humidity-dependent survival of viruses. Rather, we identify org.-based, semisolid phase states that form under equil. conditions at intermediate RH (45 to 80%). A higher-protein content causes particles to exist in a semisolid state under a wider range of RH conditions. Diffusion and, thus, disinfection kinetics are expected to be inhibited in these semisolid states. These observations suggest that org.-based, semisolid states are an important consideration to account for the recovery of virus viability at low RH obsd. in previous studies. We propose a mechanism in which the semisolid phase shields pathogens from inactivation by hindering the diffusion of solutes. This suggests that the exogenous lifetime of pathogens will depend, in part, on the org. compn. of the carrier respiratory particle and thus its origin in the respiratory tract. Furthermore, this work highlights the importance of accounting for spatial heterogeneities and time-dependent changes in the properties of aerosols and droplets undergoing evapn. in studies of pathogen viability.
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    Klein, L. K.; Luo, B.; Bluvshtein, N.; Krieger, U. K.; Schaub, A.; Glas, I.; David, S. C.; Violaki, K.; Motos, G.; Pohl, M. O.; Hugentobler, W.; Nenes, A.; Stertz, S.; Peter, T.; Kohn, T. Expiratory Aerosol PH Is Determined by Indoor Room Trace Gases and Particle Size. Proc. Natl. Acad. Sci. U.S.A. 2022, 119, e2212140119  DOI: 10.1073/pnas.2212140119
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    The National Institute for Occupational Safety and Health (NIOSH). CDC─NIOSH Pocket Guide to Chemical Hazards─Nitric acid. Time-Weighted Average (TWA) of the Permissible Exposure Limit (PEL), Legal 8-hour Limit in the United States for Exposure of an Employee 2 ppm for HNO3. https://www.cdc.gov/niosh/npg/npgd0447.html (accessed Nov 2, 2022).
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    Nicola, A. V.; McEvoy, A. M.; Straus, S. E. Roles for Endocytosis and Low PH in Herpes Simplex Virus Entry into HeLa and Chinese Hamster Ovary Cells. J. Virol. 2003, 77, 5324– 5332,  DOI: 10.1128/JVI.77.9.5324-5332.2003
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    Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells
    Nicola, Anthony V.; McEvoy, Anna M.; Straus, Stephen E.
    Journal of Virology (2003), 77 (9), 5324-5332CODEN: JOVIAM; ISSN:0022-538X. (American Society for Microbiology)
    Herpes simplex virus (HSV) infection of many cultured cells, e.g., Vero cells, can be initiated by receptor binding and pH-neutral fusion with the cell surface. Here we report that a major pathway for HSV entry into the HeLa and CHO-K1 cell lines is dependent on endocytosis and exposure to a low pH. Enveloped virions were readily detected in HeLa or receptor-expressing CHO cell vesicles by electron microscopy at <30 min postinfection. As expected, images of virus fusion with the Vero cell surface were prevalent. Treatment with energy depletion or hypertonic medium, which inhibits endocytosis, prevented uptake of HSV from the HeLa and CHO cell surface relative to uptake from the Vero cell surface. Incubation of HeLa and CHO cells with the weak base ammonium chloride or the ionophore monensin, which elevate the low pH of organelles, blocked HSV entry in a dose-dependent manner. Noncytotoxic concns. of these agents acted at an early step during infection by HSV type 1 and 2 strains. Entry mediated by the HSV receptor HveA, nectin-1, or nectin-2 was also blocked. As analyzed by fluorescence microscopy, lysosomotropic agents such as the vacuolar H+-ATPase inhibitor bafilomycin A1 blocked the delivery of virus capsids to the nuclei of the HeLa and CHO cell lines but had no effect on capsid transport in Vero cells. The results suggest that HSV can utilize two distinct entry pathways, depending on the type of cell encountered.
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    Ausar, S. F.; Rexroad, J.; Frolov, V. G.; Look, J. L.; Konar, N.; Middaugh, C. R. Analysis of the Thermal and PH Stability of Human Respiratory Syncytial Virus. Mol. Pharm. 2005, 2, 491– 499,  DOI: 10.1021/mp0500465
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    Analysis of the Thermal and pH Stability of Human Respiratory Syncytial Virus
    Ausar, Salvador F.; Rexroad, Jason; Frolov, Vladimir G.; Look, Jee L.; Konar, Nandini; Middaugh, C. Russell
    Molecular Pharmaceutics (2005), 2 (6), 491-499CODEN: MPOHBP; ISSN:1543-8384. (American Chemical Society)
    Respiratory syncytial virus (RSV) was studied as a function of pH (3-8) and temp. (10-85°) by fluorescence, CD, and high-resoln. second-deriv. absorbance spectroscopies, as well as dynamic light scattering and optical d. as a measurement of viral aggregation. The results indicate that the secondary, tertiary, and quaternary structures of RSV are both pH and temp. labile. Deriv. UV absorbance and fluorescence spectroscopy (intrinsic and extrinsic) analyses suggest that the stability of tertiary structure of RSV proteins is maximized near neutral pH. In agreement with these results, the secondary structure of RSV polypeptides seems to be more stable at pH 7-8, as evaluated by CD spectroscopy. The integrity of the viral particles studied by turbidity and dynamic light scattering also revealed that RSV is more thermally stable near neutral pH and particularly prone to aggregation below pH 6. By combination of the spectroscopic data employing a multidimensional eigenvector phase space approach, an empirical phase diagram for RSV was constructed. The pharmaceutical utility of this approach and the optimal formulation conditions are discussed.
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    Darnell, M. E. R.; Subbarao, K.; Feinstone, S. M.; Taylor, D. R. Inactivation of the Coronavirus That Induces Severe Acute Respiratory Syndrome, SARS-CoV. J. Virol. Methods 2004, 121, 85– 91,  DOI: 10.1016/j.jviromet.2004.06.006
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    Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV
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Cite this: Environ. Sci. Technol. 2023, 57, 1, 486–497
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  • Abstract

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    Figure 1

    Figure 1. Time required for 99% titer reduction of IAV, SARS-CoV-2, and human coronavirus HCoV-229E in various bulk media. Data points represent inactivation times in aqueous citric acid/Na2HPO4 buffer, SLF, or nasal mucus with pH between 7.4 and 2, measured at 22 °C. SLF concentrations correspond to water activity aw = 0.994 (1× SLF; squares), aw = 0.97 (5× SLF; stars), and aw = 0.8 (18× SLF; triangles); buffer (circles) and nasal mucus (diamonds) correspond to aw ≈ 0.99. Each experimental condition was tested in replicate with error bars indicating 95% confidence intervals. While IAV displays a pronounced reduction in infectivity around pH 5, SARS-CoV-2 develops a similar reduction only close to pH 2, and HCoV-229E is largely pH-insensitive. Solid lines are arctan fits to SLF data with aw = 0.994 (blue: IAV; red: SARS-CoV-2; and black: HCoV-229E; see eqs S26–S28). The dashed line is an arctan fit to the SLF data with aw = 0.80. The dotted line is a concentration-proportional extrapolation to aw = 0.5 (24× SLF). Upward arrows indicate insignificant change in titer over the course of the experiment, and downward arrows indicate inactivation below the level of detection at all measured times. The fitted curves below pH 2 (gray shaded area) are extrapolated with high uncertainty. Examples of measured inactivation curves are shown in Figure S3.

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    Figure 2

    Figure 2. Measured hygroscopicity cycles of an SLF particle in an EDB forced by prescribed changes in RH. The voltage required to balance the particle in the EDB against gravitational settling and aerodynamic forces is a measure of the particle’s mass-to-charge ratio, allowing the particle radius R to be estimated. (A) Two humidification cycles of an SLF particle with a dry radius R0 ≈ 9.7 μm. The experiment spanned about 2 days with slow humidity changes, allowing the thermodynamic and kinetic properties of SLF to be determined. Deliquescence/efflorescence points are marked by “Deliq/Effl”. (B) Zoom on the drying phase [red box in (A)] with salts in the droplet (mainly NaCl) efflorescing around 56% RH (black line): very fast initial crystal growth (<10 s) with rapid loss of H2O from the particle, followed by slow further crystal growth (1 h). The latter is caused by the abrupt switch from H2O diffusion to the diffusion of Na+ and Cl– ions through the viscous liquid, resulting in an ion diffusion coefficient of Dl,ions* ≈ 10–10 cm2/s. The inset (C) highlights the minute before and after efflorescence, which allows a lower bound of the H2O diffusivity to be determined, namely, Dl,H2O > 10–7 cm2/s.

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    Figure 3

    Figure 3. Evolution of physicochemical conditions within a respiratory particle leading to inactivation of trapped viruses during the transition from nasal to typical indoor air conditions, modeled with ResAM. The initial radius of the particle is 1 μm. Thermodynamic and kinetic properties are those of SLF (see Figure 2 and Table S1). The indoor air conditions are set at 20 °C and 50% RH (see Figure S10 for the corresponding depiction of physicochemical conditions at 80% RH). The exhaled air is assumed to mix into the indoor air using a turbulent eddy diffusion coefficient of 50 cm2/s (see Supporting Information, section “Mixing of the exhaled aerosol with indoor air”). The temporal evolution of gas-phase mixing ratios is shown in Figure S11. The gas-phase compositions of exhaled and typical indoor air are given in Table S4. Within 0.3 s, the particle shrinks to 0.7 μm due to rapid H2O loss, causing NaCl to effloresce (gray core). The particle then reaches 0.6 μm within 2 min due to further crystal growth, after which it slowly grows again due to coupled HNO3 and NH3 uptake and HCl loss. ResAM models the physicochemical changes in particles including (A) water activity, (B) molality of organics, (C) NO3– (resulting from the deprotonation of HNO3), (D) molality of total ammonium, (E) molality of Cl–, (F) pH, as well as inactivation of (G) IAV and (H) SARS-CoV-2 (decadal logarithm of virus titer C at time t relative to initial virus titer C0).

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    Figure 4

    Figure 4. Impact of airborne acidity on virus inactivation in expiratory particles. (A) Modeled pH value in a particle with properties of synthetic lung fluid with initially 1 μm radius exhaled into air (20 °C, 50% RH) with typical indoor composition (same as Figure 3F). (B) Same as (A), but for indoor air with NH3 reduced to 10 ppt, e.g., by means of an NH3 scrubber, reducing the time to reach pH 4 from 2 min to less than 10 s. (C) Same as (A), but in indoor air enriched to 50 ppb HNO3, reducing the time to reach pH 4 from 2 min to less than 0.5 s. (D,E) Inactivation times of IAV and SARS-CoV-2 as a function of particle radius under various conditions: indoor air with typical composition (black), depleted in NH3 to 10 ppt (light blue), enriched to 50 ppb HNO3 (dark blue), or purified air with both, HNO3 and NH3, reduced to 20 or 1% of typical indoor values (red). Whiskers show reductions of virus load to 10–4 (upper end), 10–2 (intersection with line), and 1/e (lower end). The exhaled air mixes with the indoor air by turbulent eddy diffusion (same as Figure 3); for sensitivity tests on eddy diffusivity, see Figures S14B and S15B. The gas-phase compositions of exhaled air and the various cases of indoor air shown here are defined in Table S4. (F) Mean size distribution of number emission rates of expiratory aerosol particles [dQ/dlog(R)] for breathing (solid line), speaking and singing (dotted line), and coughing (dashed line). (57) Dark gray range indicates virus radii. Light gray shading shows conditions for particles smaller than a virus, referring to an equivalent coating volume with inactivation times indicated. [Radius values in (D–F) refer to the particle size 1 s after exhalation].

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    Figure 5

    Figure 5. Airborne viral load (# infectious viruses per volume of air) and relative risk of IAV (A) and SARS-CoV-2 (B) transmission under different air treatment scenarios. Calculations are for a room (20 °C, 50% RH) with different ventilation rates (ACH) and subject to various air treatments, assuming the room to accommodate one infected person per 10 m3 of air, emitting virus-laden aerosol by normal breathing (solid curve in Figure 4E), and assuming one infectious virus per aerosol particle irrespective of size (see Figure S18 for a scenario with a size-dependent virus distribution). Steady-state viral load (left axes) is calculated as the balance of exhaled viruses and their removal by ventilation (0.1–10 ACH), deposition, and inactivation (calculated as for Figure 4D,E, starting from radius 0.05 μm, the radius of viruses). ACH affects the indoor trace gas-phase concentrations [at higher ACH, gases with predominantly outdoor sources (HNO3 and HCl) have higher concentration and gases with indoor sources (NH3, CO2, and CH3COOH) have lower concentrations]. We assume gas-phase concentrations in Table S4 to refer to 2 ACH and then calculate the gas-phase concentration for 10 ACH and 0.1 ACH by mixing with more or less outdoor air (see the Supporting Information for further details). ACH also determines the mixing speed of the exhalation plume with indoor air (see the Supporting Information). Whiskers show the uncertainty range resulting from the spread of trace gas concentrations in room air (upper limits use the least acidic composition in Table S4, i.e., the highest measured NH3 and the lowest for all acidic gases and lower limits conversely). Right axes show the transmission risk under these treatments relative to the risk in a room with typical indoor air (see Table S4) and 2 ACH (thin horizontal line). A detailed description of the relative risk calculations is given in the Supporting Information. Typical indoor air is shown by black bars, filtered air with removal of trace gases to 20% or to 1% by red bars, air with NH3 removed to 10 ppt by light blue bars, and air enriched to 50 ppb HNO3 by dark blue bars. The whiskers in the case with NH3 removal include the range of possible HNO3 release from the background aerosol particles after removing NH3 from the indoor air (see Table S4). Thick gray horizontal lines indicate the viral load and relative transmission risk in the absence of any inactivation. Results for 2 and 5 ppb HNO3, see Figure S20, results for HCoV-229E, and analyses for coughing and speaking/singing, see Figure S19.

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      Paget John; Spreeuwenberg Peter; Charu Vivek; Viboud Cecile; Charu Vivek; Taylor Robert J; Iuliano A Danielle; Bresee Joseph; Simonsen Lone; Simonsen Lone
      Journal of global health (2019), 9 (2), 020421 ISSN:.
      BACKGROUND: Until recently, the World Health Organization (WHO) estimated the annual mortality burden of influenza to be 250 000 to 500 000 all-cause deaths globally; however, a 2017 study indicated a substantially higher mortality burden, at 290 000-650 000 influenza-associated deaths from respiratory causes alone, and a 2019 study estimated 99 000-200 000 deaths from lower respiratory tract infections directly caused by influenza. Here we revisit global and regional estimates of influenza mortality burden and explore mortality trends over time and geography. METHODS: We compiled influenza-associated excess respiratory mortality estimates for 31 countries representing 5 WHO regions during 2002-2011. From these we extrapolated the influenza burden for all 193 countries of the world using a multiple imputation approach. We then used mixed linear regression models to identify factors associated with high seasonal influenza mortality burden, including influenza types and subtypes, health care and socio-demographic development indicators, and baseline mortality levels. RESULTS: We estimated an average of 389 000 (uncertainty range 294 000-518 000) respiratory deaths were associated with influenza globally each year during the study period, corresponding to ~ 2% of all annual respiratory deaths. Of these, 67% were among people 65 years and older. Global burden estimates were robust to the choice of countries included in the extrapolation model. For people <65 years, higher baseline respiratory mortality, lower level of access to health care and seasons dominated by the A(H1N1)pdm09 subtype were associated with higher influenza-associated mortality, while lower level of socio-demographic development and A(H3N2) dominance was associated with higher influenza mortality in adults ≥65 years. CONCLUSIONS: Our global estimate of influenza-associated excess respiratory mortality is consistent with the 2017 estimate, despite a different modelling strategy, and the lower 2019 estimate which only captured deaths directly caused by influenza. Our finding that baseline respiratory mortality and access to health care are associated with influenza-related mortality in persons <65 years suggests that health care improvements in low and middle-income countries might substantially reduce seasonal influenza mortality. Our estimates add to the body of evidence on the variation in influenza burden over time and geography, and begin to address the relationship between influenza-associated mortality, health and development.
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    2. 2

      Clarification of terminology: in physical chemistry, an “aerosol” is a system of colloidal particles dispersed in a fluid, such as air. An “aerosol particle” refers to one single condensed-phase element in such an ensemble, which may be solid, liquid, or mixed phase. Correspondingly, a “droplet” refers to any liquid aerosol particle, regardless of particle size. In contrast, in epidemiological or virological parlance, “aerosol” or “aerosol particle” usually means a very small (d less than 1 μm) airborne particle, whereas “droplet” is used as its larger counterpart (d greater than 1 μm). To avoid this confusion, we use the term “particle” to refer to any liquid- or mixed-phase respiratory particle of whatever size. Furthermore, we avoid the virological term “virus particle” and use “virus” instead.

      There is no corresponding record for this reference.
    3. 3
      Wang, C. C.; Prather, K. A.; Sznitman, J.; Jimenez, J. L.; Lakdawala, S. S.; Tufekci, Z.; Marr, L. C. Airborne Transmission of Respiratory Viruses. Science 2021, 373, eabd9149  DOI: 10.1126/science.abd9149
      There is no corresponding record for this reference.
    4. 4
      Smither, S. J.; Eastaugh, L. S.; Findlay, J. S.; Lever, M. S. Experimental Aerosol Survival of SARS-CoV-2 in Artificial Saliva and Tissue Culture Media at Medium and High Humidity. Emerging Microbes Infect. 2020, 9, 1415– 1417,  DOI: 10.1080/22221751.2020.1777906
      4
      Experimental aerosol survival of SARS-CoV-2 in artificial saliva and tissue culture media at medium and high humidity
      Smither, Sophie J.; Eastaugh, Lin S.; Findlay, James S.; Lever, Mark S.
      Emerging Microbes & Infections (2020), 9 (1), 1415-1417CODEN: EMIMC4; ISSN:2222-1751. (Taylor & Francis Ltd.)
      SARS-CoV-2, the causative agent of the COVID-19 pandemic, may be transmitted via airborne droplets or contact with surfaces onto which droplets have deposited. In this study, the ability of SARS-CoV-2 to survive in the dark, at two different relative humidity values and within artificial saliva, a clin. relevant matrix, was investigated. SARS-CoV-2 was found to be stable, in the dark, in a dynamic small particle aerosol under the four exptl. conditions we tested and viable virus could still be detected after 90 min. The decay rate and half-life was detd. and decay rates ranged from 0.4 to 2.27% per min and the half lives ranged from 30 to 177 min for the different conditions. This information can be used for advice and modeling and potential mitigation strategies.
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    5. 5
      Kormuth, K. A.; Lin, K.; Prussin, A. J.; Vejerano, E. P.; Tiwari, A. J.; Cox, S. S.; Myerburg, M. M.; Lakdawala, S. S.; Marr, L. C. Influenza Virus Infectivity Is Retained in Aerosols and Droplets Independent of Relative Humidity. J. Infect. Dis. 2018, 218, 739– 747,  DOI: 10.1093/infdis/jiy221
      5
      Influenza virus infectivity is retained in aerosols and droplets independent of relative humidity
      Kormuth, Karen A.; Lin, Kaisen; Prussin, Aaron J., II; Vejerano, Eric P.; Tiwari, Andrea J.; Cox, Steve S.; Myerburg, Michael M.; Lakdawala, Seema S.; Marr, Linsey C.
      Journal of Infectious Diseases (2018), 218 (5), 739-747CODEN: JIDIAQ; ISSN:1537-6613. (Oxford University Press)
      Pandemic and seasonal influenza viruses can be transmitted through aerosols and droplets, in which viruses must remain stable and infectious across a wide range of environmental conditions. Using humidity-controlled chambers, we studied the impact of relative humidity on the stability of 2009 pandemic influenza A(H1N1) virus in suspended aerosols and stationary droplets. Contrary to the prevailing paradigm that humidity modulates the stability of respiratory viruses in aerosols, we found that viruses supplemented with material from the apical surface of differentiated primary human airway epithelial cells remained equally infectious for 1 h at all relative humidities tested. This sustained infectivity was obsd. in both fine aerosols and stationary droplets. Our data suggest, for the first time, that influenza viruses remain highly stable and infectious in aerosols across a wide range of relative humidities. These results have significant implications for understanding the mechanisms of transmission of influenza and its seasonality.
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    6. 6
      Brown, J. R.; Tang, J. W.; Pankhurst, L.; Klein, N.; Gant, V.; Lai, K. M.; McCauley, J.; Breuer, J. Influenza Virus Survival in Aerosols and Estimates of Viable Virus Loss Resulting from Aerosolization and Air-Sampling. J. Hosp. Infect. 2015, 91, 278– 281,  DOI: 10.1016/j.jhin.2015.08.004
      6
      Influenza virus survival in aerosols and estimates of viable virus loss resulting from aerosolization and air-sampling
      Brown J R; Tang J W; Pankhurst L; Klein N; Breuer J; Gant V; Lai K M; McCauley J
      The Journal of hospital infection (2015), 91 (3), 278-81 ISSN:.
      Using a Collison nebulizer, aerosols of influenza (A/Udorn/307/72 H3N2) were generated within a controlled experimental chamber, from known starting virus concentrations. Air samples collected after variable suspension times were tested quantitatively using both plaque and polymerase chain reaction assays, to compare the proportion of viable virus against the amount of detectable viral RNA. These experiments showed that whereas influenza RNA copies were well preserved, the number of viable viruses decreased by a factor of 10(4)-10(5). This suggests that air-sampling studies for assessing infection control risks that detect only influenza RNA may greatly overestimate the amount of viable virus available to cause infection.
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    7. 7
      Shechmeister, I. L. Studies on the Experimental Epidemiology of Respiratory Infections: III. Certain Aspects of the Behavior of Type A Influenza Virus as an Air-Borne Cloud. J. Infect. Dis. 1950, 87, 128– 132,  DOI: 10.1093/infdis/87.2.128
      7
      Studies on the experimental epidemiology of respiratory infections. III. Certain aspects of the behavior of type A influenza virus as an air-borne cloud
      SHECHMEISTER I L
      The Journal of infectious diseases (1950), 87 (2), 128-32 ISSN:0022-1899.
      There is no expanded citation for this reference.
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    8. 8
      Hemmes, J. H.; Winkler, K. C.; Kool, S. M. Virus Survival as a Seasonal Factor in Influenza and Poliomyelitis. Nature 1960, 188, 430– 431,  DOI: 10.1038/188430a0
      8
      Virus survival as a seasonal factor in influenza and polimyelitis
      HEMMES J H; WINKLER K C; KOOL S M
      Nature (1960), 188 (), 430-1 ISSN:0028-0836.
      There is no expanded citation for this reference.
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    9. 9
      Harper, G. J. Airborne Micro-Organisms: Survival Tests with Four Viruses. J. Hyg. 1961, 59, 479– 486,  DOI: 10.1017/S0022172400039176
      9
      Airborne micro-organisms: survival tests with four viruses
      HARPER G J
      The Journal of hygiene (1961), 59 (), 479-86 ISSN:0022-1724.
      There is no expanded citation for this reference.
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    10. 10
      Schaffer, F. L.; Soergel, M. E.; Straube, D. C. Survival of Airborne Influenza Virus: Effects of Propagating Host, Relative Humidity, and Composition of Spray Fluids. Arch. Virol. 1976, 51, 263– 273,  DOI: 10.1007/BF01317930
      10
      Survival of airborne influenza virus: effects of propagating host, relative humidity, and composition of spray fluids
      Schaffer, F. L.; Soergel, M. E.; Straube, D. C.
      Archives of Virology (1976), 51 (4), 263-73CODEN: ARVIDF; ISSN:0304-8608.
      Influenza A virus, strain WSNH, propagated in bovine, human, and chick embryo cell cultures and aerosolized from the cell culture medium, was maximally stable at low relative humidity (RH), minimally stable at mid-range RH, and moderately stable at high RH. Most lots of WSNH virus propagated in embryonated eggs and aerosolized from the allantoic fluid were also least stable at mid-range RH, but 2 prepns. after multiple serial passage in eggs showed equal stability at mid-range and higher RHs. Airborne stability varied from prepn. to prepn. of virus progated both in cell culture and embryonated eggs. There was no apparent correlation between airborne stability and protein content of spray fluid >0.1 mg/ml, but 1 prepn. of lesser protein concn. was extremely unstable at 50-80% RH. Polyhydroxy compds. exerted a protective effect on airborne stability.
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    11. 11
      Schuit, M.; Gardner, S.; Wood, S.; Bower, K.; Williams, G.; Freeburger, D.; Dabisch, P. The Influence of Simulated Sunlight on the Inactivation of Influenza Virus in Aerosols. J. Infect. Dis. 2020, 221, 372– 378,  DOI: 10.1093/infdis/jiz582
      11
      The Influence of Simulated Sunlight on the Inactivation of Influenza Virus in Aerosols
      Schuit Michael; Gardner Sierra; Wood Stewart; Bower Kristin; Williams Greg; Freeburger Denise; Dabisch Paul
      The Journal of infectious diseases (2020), 221 (3), 372-378 ISSN:.
      BACKGROUND: Environmental parameters, including sunlight levels, are known to affect the survival of many microorganisms in aerosols. However, the impact of sunlight on the survival of influenza virus in aerosols has not been previously quantified. METHODS: The present study examined the influence of simulated sunlight on the survival of influenza virus in aerosols at both 20% and 70% relative humidity using an environmentally controlled rotating drum aerosol chamber. RESULTS: Measured decay rates were dependent on the level of simulated sunlight, but they were not significantly different between the 2 relative humidity levels tested. In darkness, the average decay constant was 0.02 ± 0.06 min-1, equivalent to a half-life of 31.6 minutes. However, at full intensity simulated sunlight, the mean decay constant was 0.29 ± 0.09 min-1, equivalent to a half-life of approximately 2.4 minutes. CONCLUSIONS: These results are consistent with epidemiological findings that sunlight levels are inversely correlated with influenza transmission, and they can be used to better understand the potential for the virus to spread under varied environmental conditions.
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    12. 12
      Schuit, M.; Ratnesar-Shumate, S.; Yolitz, J.; Williams, G.; Weaver, W.; Green, B.; Miller, D.; Krause, M.; Beck, K.; Wood, S.; Holland, B.; Bohannon, J.; Freeburger, D.; Hooper, I.; Biryukov, J.; Altamura, L. A.; Wahl, V.; Hevey, M.; Dabisch, P. Airborne SARS-CoV-2 Is Rapidly Inactivated by Simulated Sunlight. J. Infect. Dis. 2020, 222, 564– 571,  DOI: 10.1093/infdis/jiaa334
      12
      Airborne SARS-CoV-2 is rapidly inactivated by simulated sunlight
      Schuit, Michael; Ratnesar-Shumate, Shanna; Yolitz, Jason; Williams, Gregory; Weaver, Wade; Green, Brian; Miller, David; Krause, Melissa; Beck, Katie; Wood, Stewart; Holland, Brian; Bohannon, Jordan; Freeburger, Denise; Hooper, Idris; Biryukov, Jennifer; Altamura, Louis A.; Wahl, Victoria; Hevey, Michael; Dabisch, Paul
      Journal of Infectious Diseases (2020), 222 (4), 564-571CODEN: JIDIAQ; ISSN:1537-6613. (Oxford University Press)
      Aerosols represent a potential transmission route of COVID-19. This study examd. effect of simulated sunlight, relative humidity, and suspension matrix on stability of SARS-CoV-2 in aerosols. Simulated sunlight and matrix significantly affected decay rate of the virus. Relative humidity alone did not affect the decay rate; however, minor interactions between relative humidity and other factors were obsd. Mean decay rates (± SD) in simulated saliva, under simulated sunlight levels representative of late winter/early fall and summer were 0.121 ± 0.017 min-1 (90% loss, 19 min) and 0.306 ± 0.097 min-1 (90% loss, 8 min), resp. Mean decay rate without simulated sunlight across all relative humidity levels was 0.008 ± 0.011 min-1 (90% loss, 286 min). These results suggest that the potential for aerosol transmission of SARS-CoV-2 may be dependent on environmental conditions, particularly sunlight. These data may be useful to inform mitigation strategies to minimize the potential for aerosol transmission.
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    13. 13
      Dabisch, P.; Schuit, M.; Herzog, A.; Beck, K.; Wood, S.; Krause, M.; Miller, D.; Weaver, W.; Freeburger, D.; Hooper, I.; Green, B.; Williams, G.; Holland, B.; Bohannon, J.; Wahl, V.; Yolitz, J.; Hevey, M.; Ratnesar-Shumate, S. The Influence of Temperature, Humidity, and Simulated Sunlight on the Infectivity of SARS-CoV-2 in Aerosols. Aerosol Sci. Technol. 2020, 55, 142,  DOI: 10.1080/02786826.2020.1829536
      There is no corresponding record for this reference.
    14. 14
      van Doremalen, N.; Bushmaker, T.; Morris, D. H.; Holbrook, M. G.; Gamble, A.; Williamson, B. N.; Tamin, A.; Harcourt, J. L.; Thornburg, N. J.; Gerber, S. I.; Lloyd-Smith, J. O.; de Wit, E.; Munster, V. J. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N. Engl. J. Med. 2020, 382, 1564– 1567,  DOI: 10.1056/NEJMc2004973
      14
      Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1
      van Doremalen Neeltje; Bushmaker Trenton; Holbrook Myndi G; Williamson Brandi N; de Wit Emmie; Munster Vincent J; Morris Dylan H; Gamble Amandine; Tamin Azaibi; Harcourt Jennifer L; Thornburg Natalie J; Gerber Susan I; Lloyd-Smith James O
      The New England journal of medicine (2020), 382 (16), 1564-1567 ISSN:.
      There is no expanded citation for this reference.
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    15. 15
      Ijaz, M. K.; Brunner, A. H.; Sattar, S. A.; Nair, R. C.; Johnson-Lussenburg, C. M. Survival Characteristics of Airborne Human Coronavirus 229E. J. Gen. Virol. 1985, 66, 2743– 2748,  DOI: 10.1099/0022-1317-66-12-2743
      15
      Survival characteristics of airborne human coronavirus 229E
      Ijaz M K; Brunner A H; Sattar S A; Nair R C; Johnson-Lussenburg C M
      The Journal of general virology (1985), 66 ( Pt 12) (), 2743-8 ISSN:0022-1317.
      The survival of airborne human coronavirus 229E (HCV/229E) was studied under different conditions of temperature (20 +/- 1 degree C and 6 +/- 1 degree C) and low (30 +/- 5%), medium (50 +/- 5%) or high (80 +/- 5%) relative humidities (RH). At 20 +/- 1 degree C, aerosolized HCV/229E was found to survive best at 50% RH with a half-life of 67.33 +/- 8.24 h while at 30% RH the virus half-life was 26.76 +/- 6.21 h. At 50% RH nearly 20% infectious virus was still detectable at 6 days. High RH at 20 +/- 1 degree C, on the other hand, was found to be the least favourable to the survival of aerosolized virus and under these conditions the virus half-life was only about 3 h; no virus could be detected after 24 h in aerosol. At 6 +/- 1 degree C, in either 50% or 30% RH conditions, the survival of HCV/229E was significantly enhanced, with the decay pattern essentially similar to that seen at 20 +/- 1 degree C. At low temperature and high RH (80%), however, the survival pattern was completely reversed, with the HCV/229E half-life increasing to 86.01 +/- 5.28 h, nearly 30 times that found at 20 +/- 1 degree C and high RH. Although optimal survival at 6 degree C still occurred at 50% RH, the pronounced stabilizing effect of low temperature on the survival of HCV/229E at high RH indicates that the role of the environment on the survival of viruses in air may be more complex and significant than previously thought.
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    16. 16
      Marr, L. C.; Tang, J. W.; Van Mullekom, J.; Lakdawala, S. S. Mechanistic Insights into the Effect of Humidity on Airborne Influenza Virus Survival, Transmission and Incidence. J. R. Soc., Interface 2019, 16, 20180298,  DOI: 10.1098/rsif.2018.0298
      16
      Mechanistic insights into the effect of humidity on airborne influenza virus survival, transmission and incidence
      Marr, Linsey C.; Tang, Julian W.; Van Mullekom, Jennifer; Lakdawala, Seema S.
      Journal of the Royal Society, Interface (2019), 16 (150), 20180298CODEN: JRSICU; ISSN:1742-5662. (Royal Society)
      A review. Influenza incidence and seasonality, along with virus survival and transmission, appear to depend at least partly on humidity, and recent studies have suggested that abs. humidity (AH) is more important than relative humidity (RH) in modulating obsd. patterns. In this perspective article, we re-evaluate studies of influenza virus survival in aerosols, transmission in animal models and influenza incidence to show that the combination of temp. and RH is equally valid as AH as a predictor. Collinearity must be considered, as higher levels of AH are only possible at higher temps., where it is well established that virus decay is more rapid. In studies of incidence that employ meteorol. data, outdoor AH may be serving as a proxy for indoor RH in temperate regions during the wintertime heating season. Finally, we present a mechanistic explanation based on droplet evapn. and its impact on droplet physics and chem. for why RH is more likely than AH to modulate virus survival and transmission.
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    17. 17
      Lin, K.; Marr, L. C. Humidity-Dependent Decay of Viruses, but Not Bacteria, in Aerosols and Droplets Follows Disinfection Kinetics. Environ. Sci. Technol. 2020, 54, 1024– 1032,  DOI: 10.1021/acs.est.9b04959
      17
      Humidity-Dependent Decay of Viruses, but Not Bacteria, in Aerosols and Droplets Follows Disinfection Kinetics
      Lin, Kaisen; Marr, Linsey C.
      Environmental Science & Technology (2020), 54 (2), 1024-1032CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
      The transmission of some infectious diseases requires that pathogens can survive (i.e., remain infectious) in the environment, outside the host. Relative humidity (RH) is known to affect the survival of some microorganisms in the environment; however, the mechanism underlying the relationship has not been explained, particularly for viruses. We investigated the effects of RH on the viability of bacteria and viruses in both suspended aerosols and stationary droplets using traditional culture-based approaches. Results showed that viability of bacteria generally decreased with decreasing RH. Viruses survived well at RHs lower than 33% and at 100%, whereas their viability was reduced at intermediate RHs. We then explored the evapn. rate of droplets consisting of culture media and the resulting changes in solute concns. over time; as water evaps. from the droplets, solutes such as sodium chloride in the media become more concd. Based on the results, we suggest that inactivation of bacteria is influenced by osmotic pressure resulting from elevated concns. of salts as droplets evap. We propose that the inactivation of viruses is governed by the cumulative dose of solutes or the product of concn. and time, as in disinfection kinetics. These findings emphasize that evapn. kinetics play a role in modulating the survival of microorganisms in droplets.
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    18. 18
      Morris, D. H.; Yinda, K. C.; Gamble, A.; Rossine, F. W.; Huang, Q.; Bushmaker, T.; Fischer, R. J.; Matson, M. J.; Van Doremalen, N.; Vikesland, P. J.; Marr, L. C.; Munster, V. J.; Lloyd-Smith, J. O. Mechanistic Theory Predicts the Effects of Temperature and Humidity on Inactivation of SARS-CoV-2 and Other Enveloped Viruses. eLife 2021, 10, e65902  DOI: 10.7554/eLife.65902
      18
      Mechanistic theory predicts the effects of temperature and humidity on inactivation of SARS-CoV-2 and other enveloped viruses
      Morris, Dylan H.; Yinda, Kwe Claude; Gamble, Amandine; Rossine, Fernando W.; Huang, Qishen; Bushmaker, Trenton; Fischer, Robert J.; Matson, M. Jeremiah; Van Doremalen, Neeltje; Vikesland, Peter J.; Marr, Linsey C.; Munster, Vincent J.; Lloyd-Smith, James O.
      eLife (2021), 10 (), e65902CODEN: ELIFA8; ISSN:2050-084X. (eLife Sciences Publications Ltd.)
      Ambient temp. and humidity strongly affect inactivation rates of enveloped viruses, but a mechanistic, quant. theory of these effects has been elusive. We measure the stability of SARS-CoV-2 on an inert surface at nine temp. and humidity conditions and develop a mechanistic model to explain and predict how temp. and humidity alter virus inactivation. We fiend SARS-CoV-2 survives longest at low temps. and extreme relative humidities (RH); median estd. virus half-life is >24 h at 10°C and 40% RH, but -1.5 h at 27°C and 65% RH. Our mechanistic model uses fundamental chem. to explain why inactivation rate increases with increased temp. and shows a U-shaped dependence on RH. The model accurately predicts existing measurements of five different human coronaviruses, suggesting that shared mechanisms may affect stability for many viruses. The results indicate scenarios of high transmission risk, point to mitigation strategies, and advance the mechanistic study of virus transmission.
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    19. 19
      Niazi, S.; Groth, R.; Cravigan, L.; He, C.; Tang, J. W.; Spann, K.; Johnson, G. R. Susceptibility of an Airborne Common Cold Virus to Relative Humidity. Environ. Sci. Technol. 2021, 55, 499– 508,  DOI: 10.1021/acs.est.0c06197
      19
      Susceptibility of an Airborne Common Cold Virus to Relative Humidity
      Niazi, Sadegh; Groth, Robert; Cravigan, Luke; He, Congrong; Tang, Julian W.; Spann, Kirsten; Johnson, Graham R.
      Environmental Science & Technology (2021), 55 (1), 499-508CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
      The viability of airborne respiratory viruses varies with ambient relative humidity (RH). Numerous contrasting reports spanning several viruses have failed to identify the mechanism underlying this dependence. We hypothesized that an "efflorescence/deliquescence divergent infectivity" (EDDI) model accurately predicts the RH-dependent survival of airborne human rhinovirus-16 (HRV-16). We measured the efflorescence and deliquescence RH (RHE and RHD, resp.) of aerosols nebulized from a protein-enriched saline carrier fluid simulating the human respiratory fluid and found the RH range of the aerosols' hygroscopic hysteresis zone (RHE-D) to be 38-68%, which encompasses the preferred RH for indoor air (40-60%). The carrier fluid contg. HRV-16 was nebulized into the sub-hysteresis zone (RH<E) or super-hysteresis zone (RH>D) air, to set the aerosols to the effloresced/solid or deliquesced/liq. state before transitioning the RH into the intermediate hysteresis zone. The surviving fractions (SFs) of the virus were then measured 15 min post nebulization. SFs were also measured for aerosols introduced directly into the RH<E, RHE-D, and RH>D zones without transition. SFs for transitioned aerosols in the hysteresis zone were higher for effloresced (0.17 ± 0.02) than for deliquesced (0.005 ± 0.005) aerosols. SFs for nontransitioned aerosols in the RH<E, RHE-D, and RH>D zones were 0.18 ± 0.06, 0.05 ± 0.02, and 0.20 ± 0.05, resp., revealing a V-shaped SF/RH dependence. The EDDI model's prediction of enhanced survival in the hysteresis zone for effloresced carrier aerosols was confirmed.
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    20. 20
      Niazi, S.; Short, K. R.; Groth, R.; Cravigan, L.; Spann, K.; Ristovski, Z.; Johnson, G. R. Humidity-Dependent Survival of an Airborne Influenza A Virus: Practical Implications for Controlling Airborne Viruses. Environ. Sci. Technol. Lett. 2021, 8, 412– 418,  DOI: 10.1021/acs.estlett.1c00253
      20
      Humidity-Dependent Survival of an Airborne Influenza A Virus: Practical Implications for Controlling Airborne Viruses
      Niazi, Sadegh; Short, Kirsty R.; Groth, Robert; Cravigan, Luke; Spann, Kirsten; Ristovski, Zoran; Johnson, Graham R.
      Environmental Science & Technology Letters (2021), 8 (5), 412-418CODEN: ESTLCU; ISSN:2328-8930. (American Chemical Society)
      Relative humidity (RH) can affect influenza A virus (IAV) survival. However, the mechanism driving this relationship is unknown. We hypothesized that the RH-dependent survival of airborne IAV could be predicted by the efflorescence/deliquescence divergent infectivity (EDDI) hypothesis. We detd. three distinct RH response zones based on the hygroscopic growth factor of carrier aerosols. These zones were classified as the super-deliquescence zone (RH > 75%), the hysteresis zone (43% < RH < 75%), and the sub-efflorescence zone (RH < 43%). We added IAV (H3N2) to protein-enriched saline and aerosolized it into sub-efflorescence or super-deliquescence zone air, yielding aerosols in the effloresced or noneffloresced state, resp. We then adjusted the RH to an ergonomically comfortable RH (60%). Fifteen minutes post-aerosolization, the surviving fractions (arithmetic means ± std. errors) of virus were higher in effloresced aerosols (9.5 ± 0.5%) than in non-effloresced aerosols (0.40 ± 0.05%). A virus suspension was also aerosolized directly into air within the super-deliquescence, hysteresis, and sub-efflorescence zones to assess the impact of the sudden change in RH from an initial 100% satd. RH to these zonal ranges. Fifteen minutes post-aerosolization, the surviving fractions were 3 ± 0.4%, 2 ± 0.1%, and 12 ± 2%, resp. Survival following gradual adaptation to the hysteresis zone RH range was sustained in effloresced and reduced in the non-effloresced aerosols. The EDDI model predicted the survival of IAV under seasonal conditions, offering strategies for controlling indoor air infection.
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    21. 21
      Yang, W.; Elankumaran, S.; Marr, L. C. Relationship between Humidity and Influenza A Viability in Droplets and Implications for Influenza’s Seasonality. PloS One 2012, 7, e46789  DOI: 10.1371/journal.pone.0046789
      21
      Relationship between humidity and influenza a viability in droplets and implications for influenza's seasonality
      Yang, Wan; Elankumaran, Subbiah; Marr, Linsey C.
      PLoS One (2012), 7 (10), e46789CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
      Humidity has been assocd. with influenza's seasonality, but the mechanisms underlying the relationship remain unclear. There is no consistent explanation for influenza's transmission patterns that applies to both temperate and tropical regions. This study aimed to det. the relationship between ambient humidity and viability of the influenza A virus (IAV) during transmission between hosts and to explain the mechanisms underlying it. We measured the viability of IAV in droplets consisting of various model media, chosen to isolate effects of salts and proteins found in respiratory fluid, and in human mucus, at relative humidities (RH) ranging from 17% to 100%. In all media and mucus, viability was highest when RH was either close to 100% or below ∼50%. When RH decreased from 84% to 50%, the relationship between viability and RH depended on droplet compn.: viability decreased in saline solns., did not change significantly in solns. supplemented with proteins, and increased dramatically in mucus. Addnl., viral decay increased linearly with salt concn. in saline solns. but not when they were supplemented with proteins. There appear to be three regimes of IAV viability in droplets, defined by humidity: physiol. conditions (∼100% RH) with high viability, concd. conditions (50% to near 100% RH) with lower viability depending on the compn. of media, and dry conditions (<50% RH) with high viability. This paradigm could help resolve conflicting findings in the literature on the relationship between IAV viability in aerosols and humidity, and results in human mucus could help explain influenza's seasonality in different regions.
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    22. 22
      Weber, R. J.; Guo, H.; Russell, A. G.; Nenes, A. High Aerosol Acidity despite Declining Atmospheric Sulfate Concentrations over the Past 15 Years. Nat. Geosci. 2016, 9, 282– 285,  DOI: 10.1038/ngeo2665
      22
      High aerosol acidity despite declining atmospheric sulfate concentrations over the past 15 years
      Weber, Rodney J.; Guo, Hongyu; Russell, Armistead G.; Nenes, Athanasios
      Nature Geoscience (2016), 9 (4), 282-285CODEN: NGAEBU; ISSN:1752-0894. (Nature Publishing Group)
      Particle acidity affects aerosol concns., chem. compn. and toxicity. Sulfate is often the main acid component of aerosols, and largely dets. the acidity of fine particles under 2.5 μm in diam., PM2.5. Over the past 15 years, atm. sulfate concns. in the southeastern United States have decreased by 70%, whereas ammonia concns. have been steady. Similar trends are occurring in many regions globally. Aerosol ammonium nitrate concns. were assumed to increase to compensate for decreasing sulfate, which would result from increasing neutrality. Here we use obsd. gas and aerosol compn., humidity, and temp. data collected at a rural southeastern US site in June and July 2013 (ref. 1), and a thermodn. model that predicts pH and the gas-particle equil. concns. of inorg. species from the observations to show that PM2.5 at the site is acidic. PH buffering by partitioning of ammonia between the gas and particle phases produced a relatively const. particle pH of 0-2 throughout the 15 years of decreasing atm. sulfate concns., and little change in particle ammonium nitrate concns. We conclude that the redns. in aerosol acidity widely anticipated from sulfur redns., and expected acidity-related health and climate benefits, are unlikely to occur until atm. sulfate concns. reach near pre-anthropogenic levels.
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    23. 23
      Scholtissek, C. Stability of Infectious Influenza A Viruses to Treatment at Low PH and Heating. Arch. Virol. 1985, 85, 1– 11,  DOI: 10.1007/BF01317001
      23
      Stability of infectious influenza A viruses to treatment at low pH and heating
      Scholtissek C
      Archives of virology (1985), 85 (1-2), 1-11 ISSN:0304-8608.
      We have measured the infectivity of influenza A virus strains grown either in embryonated eggs or in chick embryo cells in culture after treatment at low pH. At pH values at which hemolysis occurs there was an irreversible loss of infectivity. The threshold pH, at which the infectivity was lost, depended on the hemagglutinin subtype of the virus strain. All H5 and H7 strains tested were extremely labile at low pH. In contrast, all H3 strains were relatively stable, independent of the species from which the viruses were isolated. With several H1 viruses the hemagglutination (HA) activity was irreversibly lost at intermediate pH values causing inactivation of infectivity. Strains with noncleaved hemagglutinins were much more stable. These observations might explain why duck influenza viruses can easily survive in lake water and wet faeces, and multiply in the intestinal tract, where trypsin is present. There are also significant differences in heat stability exhibited by influenza A strains. In contrast to pH stability this is not a specific trait of the hemagglutinin, since it can be influenced by reassortment. There is no correlation between the stability of infectivity at low pH and heat.
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    24. 24
      Yang, W.; Marr, L. C. Mechanisms by Which Ambient Humidity May Affect Viruses in Aerosols. Appl. Environ. Microbiol. 2012, 78, 6781– 6788,  DOI: 10.1128/AEM.01658-12
      24
      Mechanisms by which ambient humidity may affect viruses in aerosols
      Yang, Wan; Marr, Linsey C.
      Applied and Environmental Microbiology (2012), 78 (19), 6781-6788CODEN: AEMIDF; ISSN:0099-2240. (American Society for Microbiology)
      A review. Many airborne viruses have been shown to be sensitive to ambient humidity, yet the mechanisms responsible for this phenomenon remain elusive. We review multiple hypotheses, including water activity, surface inactivation, and salt toxicity, that may account for the assocn. between humidity and viability of viruses in aerosols. We assess the evidence and limitations for each hypothesis based on findings from virol., aerosol science, chem., and physics. In addn., we hypothesize that changes in pH within the aerosol that are induced by evapn. may trigger conformational changes of the surface glycoproteins of enveloped viruses and subsequently compromise their infectivity. This hypothesis may explain the differing responses of enveloped viruses to humidity. The precise mechanisms underlying the relationship remain largely unverified, and attaining a complete understanding of them will require an interdisciplinary approach.
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    25. 25
      Pye, H. O. T.; Nenes, A.; Alexander, B.; Ault, A. P.; Barth, M. C.; Clegg, S. L.; Collett, J. L., Jr.; Fahey, K. M.; Hennigan, C. J.; Herrmann, H.; Kanakidou, M.; Kelly, J. T.; Ku, I.-T.; McNeill, V. F.; Riemer, N.; Schaefer, T.; Shi, G.; Tilgner, A.; Walker, J. T.; Wang, T.; Weber, R.; Xing, J.; Zaveri, R. A.; Zuend, A. The Acidity of Atmospheric Particles and Clouds. Atmos. Chem. Phys. 2020, 20, 4809– 4888,  DOI: 10.5194/acp-20-4809-2020
      25
      The acidity of atmospheric particles and clouds
      Pye, Havala O. T.; Nenes, Athanasios; Alexander, Becky; Ault, Andrew P.; Barth, Mary C.; Clegg, Simon L.; Collett, Jeffrey L., Jr.; Fahey, Kathleen M.; Hennigan, Christopher J.; Herrmann, Hartmut; Kanakidou, Maria; Kelly, James T.; Ku, I-Ting; McNeill, V. Faye; Riemer, Nicole; Schaefer, Thomas; Shi, Guoliang; Tilgner, Andreas; Walker, John T.; Wang, Tao; Weber, Rodney; Xing, Jia; Zaveri, Rahul A.; Zuend, Andreas
      Atmospheric Chemistry and Physics (2020), 20 (8), 4809-4888CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
      Acidity, defined as pH, is a central component of aq. chem. In the atm., the acidity of condensed phases (aerosol particles, cloud water, and fog droplets) governs the phase partitioning of semivolatile gases such as HNO3, NH3, HCl, and org. acids and bases as well as chem. reaction rates. It has implications for the atm. lifetime of pollutants, deposition, and human health. Despite its fundamental role in atm. processes, only recently has this field seen a growth in the no. of studies on particle acidity. Even with this growth, many fine-particle pH ests. must be based on thermodn. model calcns. since no operational techniques exist for direct measurements. Current information indicates acidic fine particles are ubiquitous, but observationally constrained pH ests. are limited in spatial and temporal coverage. Clouds and fogs are also generally acidic, but to a lesser degree than particles, and have a range of pH that is quite sensitive to anthropogenic emissions of sulfur and nitrogen oxides, as well as ambient ammonia. Historical measurements indicate that cloud and fog droplet pH has changed in recent decades in response to controls on anthropogenic emissions, while the limited trend data for aerosol particles indicate acidity may be relatively const. due to the semivolatile nature of the key acids and bases and buffering in particles. This paper reviews and synthesizes the current state of knowledge on the acidity of atm. condensed phases, specifically particles and cloud droplets. It includes recommendations for estg. acidity and pH, std. nomenclature, a synthesis of current pH ests. based on observations, and new model calcns. on the local and global scale.
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    26. 26
      Oswin, H. P.; Haddrell, A. E.; Otero-Fernandez, M.; Mann, J. F. S.; Cogan, T. A.; Hilditch, T. G.; Tian, J.; Hardy, D. A.; Hill, D. J.; Finn, A.; Davidson, A. D.; Reid, J. P. The Dynamics of SARS-CoV-2 Infectivity with Changes in Aerosol Microenvironment. Proc. Natl. Acad. Sci. U.S.A. 2022, 119, e2200109119  DOI: 10.1073/pnas.2200109119
      There is no corresponding record for this reference.
    27. 27
      Huang, Y. The SARS Epidemic and Its Aftermath in China: A Political Perspective. In Learning from SARS─Preparing for the Next Disease Outbreak: Workshop Summary; Institute of Medicine, The National Academies Press: Washington DC, 2004; pp 116– 136.
      There is no corresponding record for this reference.
    28. 28
      Nah, T.; Guo, H.; Sullivan, A. P.; Chen, Y.; Tanner, D. J.; Nenes, A.; Russell, A.; Ng, N.; Huey, L.; Weber, R. J. Characterization of Aerosol Composition, Aerosol Acidity, and Organic Acid Partitioning at an Agriculturally Intensive Rural Southeastern US Site. Atmos. Chem. Phys. 2018, 18, 11471– 11491,  DOI: 10.5194/acp-18-11471-2018
      28
      Characterization of aerosol composition, aerosol acidity, and organic acid partitioning at an agriculturally intensive rural southeastern US site
      Nah, Theodora; Guo, Hongyu; Sullivan, Amy P.; Chen, Yunle; Tanner, David J.; Nenes, Athanasios; Russell, Armistead; Ng, Nga Lee; Huey, L. Gregory; Weber, Rodney J.
      Atmospheric Chemistry and Physics (2018), 18 (15), 11471-11491CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
      The implementation of stringent emission regulations has resulted in the decline of anthropogenic pollutants including sulfur dioxide (SO2), nitrogen oxides (NOx), and carbon monoxide (CO). In contrast, ammonia (NH3) emissions are largely unregulated, with emissions projected to increase in the future. We present real-time aerosol and gas measurements from a field study conducted in an agriculturally intensive region in the southeastern US during the fall of 2016 to investigate how NH3 affects particle acidity and secondary org. aerosol (SOA) formation via the gas-particle partitioning of semi-volatile org. acids. Particle water and pH were detd. using the ISORROPIA II thermodn. model and validated by comparing predicted inorg. HNO3-NO3- and NH3-NHC4 gas-particle partitioning ratios with measured values. Our results showed that despite the high NH3 concns. (av. 8.1±5.2 ppb), PM1 was highly acidic with pH values ranging from 0.9 to 3.8, and an av. pH of 2.2±0.6. PM1 pH varied by approx. 1.4 units diurnally. Measured particle-phase water-sol. org. acids were on av. 6% of the total non-refractory PM1 org. aerosol mass. The measured oxalic acid gas-particle partitioning ratios were in good agreement with their corresponding thermodn. predictions, calcd. based on oxalic acid's physicochem. properties, ambient temp., particle water, and pH.
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    29. 29
      Brauer, M.; Koutrakis, P.; Keeler, G. J.; Spengler, J. D. Indoor and Outdoor Concentrations of Inorganic Acidic Aerosols and Gases. J. Air Waste Manage. Assoc. 1991, 41, 171– 181,  DOI: 10.1080/10473289.1991.10466834
      29
      Indoor and outdoor concentrations of inorganic acidic aerosols and gases
      Brauer, Michael; Koutrakis, Petros; Keeler, Gerald J.; Spengler, John D.
      Journal of the Air & Waste Management Association (1990-1992) (1991), 41 (2), 171-81CODEN: JAWAEB; ISSN:1047-3289.
      Annular denuder-filter pack sampling systems were used to make indoor and outdoor measurements of aerosol strong H+, SO42-, NH4+, NO3-, and NO2-, and the gaseous pollutants SO2, HNO3, HONO, and NH3 during summer and winter periods in Boston, Massachusetts. Outdoor levels of SO2, HNO3, H+, and SO42- exceeded their indoor concns. during both seasons. Winter indoor/outdoor ratios were lower than during the summer, probably due to lower air exchange rates during the winter period. During both monitoring periods, indoor/outdoor ratios of aerosol strong H+ were 40-50% of the indoor/outdoor SO42- ratio. Since aerosol strong acidity is typically assocd. with SO42-, this finding is indicative of neutralization of the acidic aerosol by the higher indoor NH3 levels. Geometric mean indoor/outdoor NH3 ratios of 3.5 and 23 resp. were measured for the summer and winter sampling periods. For HONO, NH3, NH4+, and NO2-, indoor concns. were significantly higher than ambient levels. Indoor levels of NO3- were slightly less than outdoor concns.
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    30. 30
      Nazaroff, W. W.; Weschler, C. J. Indoor Acids and Bases. Indoor Air 2020, 30, 559– 644,  DOI: 10.1111/ina.12670
      30
      Indoor acids and bases
      Nazaroff, William W.; Weschler, Charles J.
      Indoor Air (2020), 30 (4), 559-644CODEN: INAIE5; ISSN:1600-0668. (Wiley-Blackwell)
      A review. Numerous acids and bases influence indoor air quality. The most abundant of these species are CO2 (acidic) and NH3 (basic), both emitted by building occupants. Other prominent inorg. acids are HNO3, HONO, SO2, H2SO4, HCl, and HOCl. Prominent org. acids include formic, acetic, and lactic; nicotine is a noteworthy org. base. Sources of N-, S-, and Cl-contg. acids can include ventilation from outdoors, indoor combustion, consumer product use, and chem. reactions. Org. acids are commonly more abundant indoors than outdoors, with indoor sources including occupants, wood, and cooking. Beyond NH3 and nicotine, other noteworthy bases include inorg. and org. amines. Acids and bases partition indoors among the gas-phase, airborne particles, bulk water, and surfaces; relevant thermodn. parameters governing the partitioning are the acid-dissocn. const. (Ka), Henry's law const. (KH), and the octanol-air partition coeff. (Koa). Condensed-phase water strongly influences the fate of indoor acids and bases and is also a medium for chem. interactions. Indoor surfaces can be large reservoirs of acids and bases. This extensive review of the state of knowledge establishes a foundation for future inquiry to better understand how acids and bases influence the suitability of indoor environments for occupants, cultural artifacts, and sensitive equipment.
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    31. 31
      Ampollini, L.; Katz, E. F.; Bourne, S.; Tian, Y.; Novoselac, A.; Goldstein, A. H.; Lucic, G.; Waring, M. S.; DeCarlo, P. F. Observations and Contributions of Real-Time Indoor Ammonia Concentrations during HOMEChem. Environ. Sci. Technol. 2019, 53, 8591– 8598,  DOI: 10.1021/acs.est.9b02157
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      Observations and Contributions of Real-Time Indoor Ammonia Concentrations during HOMEChem
      Ampollini, Laura; Katz, Erin F.; Bourne, Stephen; Tian, Yilin; Novoselac, Atila; Goldstein, Allen H.; Lucic, Gregor; Waring, Michael S.; DeCarlo, Peter F.
      Environmental Science & Technology (2019), 53 (15), 8591-8598CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
      Although NH3 usually occurs outdoors at 1-5 ppb concns., indoor NH3 concns. can be much higher. Indoor NH3 is strongly emitted by cleaning products, tobacco smoke, building materials, and humans. Due to its high reactivity, water soly., and tendency to sorb to surfaces, NH2 os difficult to measure; hence, a comprehensive evaluation of indoor NH3 concns. is under-studied. During HOMEChem, a comprehensive indoor chem. study in a test house in June 2018, real-time indoor NH3 concns. were measured using cavity ring-down spectroscopy. A mean unoccupied background concn. of 32 ppb was obsd.; NH3 concns. were enhanced by cooking, cleaning, and occupancy, reaching max. concns. of 130, 1592, and 99 ppb, resp. NH3 concns. were strongly affected by indoor temp. and HVAC (heating, ventilation, air conditioning) operations. In the absence of activity-based sources, HVAC operation was the main indoor NH3 concn. modulator.
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    32. 32
      Vaughan, J.; Ngamtrakulpanit, L.; Pajewski, T. N.; Turner, R.; Nguyen, T. A.; Smith, A.; Urban, P.; Hom, S.; Gaston, B.; Hunt, J. Exhaled Breath Condensate PH Is a Robust and Reproducible Assay of Airway Acidity. Eur. Respir. J. 2003, 22, 889– 894,  DOI: 10.1183/09031936.03.00038803
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      Exhaled breath condensate pH is a robust and reproducible assay of airway acidity
      Vaughan J; Ngamtrakulpanit L; Pajewski T N; Turner R; Nguyen T A; Smith A; Urban P; Hom S; Gaston B; Hunt J
      The European respiratory journal (2003), 22 (6), 889-94 ISSN:0903-1936.
      Exhaled breath condensate (EBC) pH is low in several lung diseases and it normalises with therapy. The current study examined factors relevant to EBC pH monitoring. Intraday and intraweek variability were studied in 76 subjects. The pH of EBC collected orally and from isolated lower airways was compared in an additional 32 subjects. Effects of ventilatory pattern (hyperventilation/hypoventilation), airway obstruction after methacholine, temperature (-44 to +13 degrees C) and duration of collection (2-7 min), and duration of sample storage (up to 2 yrs) were examined. All samples were collected with a disposable condensing device, and de-aerated with argon until pH measurement stabilised. Mean EBC pH (n=76 subjects, total samples=741) was 7.7+/-0.49 (mean+/-SD). Mean intraweek and intraday coefficients of variation were 4.5% and 3.5%. Control of EBC pH appears to be at the level of the lower airway. Temperature of collection, duration of collection and storage, acute airway obstruction, subject age, saliva pH, and profound hyperventilation and hypoventilation had no effect on EBC pH. The current authors conclude that in health, exhaled breath condensate pH is slightly alkaline, held in a narrow range, and is controlled by lower airway source fluid. Measurement of exhaled breath condensate pH is a simple, robust, reproducible and relevant marker of disease.
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    33. 33
      Colberg, C. A.; Krieger, U. K.; Peter, T. Morphological Investigations of Single Levitated H2SO4/NH3/H2O Aerosol Particles during Deliquescence/Efflorescence Experiments. J. Phys. Chem. A 2004, 108, 2700– 2709,  DOI: 10.1021/jp037628r
      33
      Morphological investigations of single levitated H2SO4/NH3/H2O aerosol particles during deliquescence/efflorescence experiments
      Colberg, Christina A.; Krieger, Ulrich K.; Peter, Thomas
      Journal of Physical Chemistry A (2004), 108 (14), 2700-2709CODEN: JPCAFH; ISSN:1089-5639. (American Chemical Society)
      In an electrodynamic particle trap, expts. with single levitated H2SO4/NH3/H2O aerosol particles have been performed under atm. conditions. Four anal. methods provide independent information on the aerosol compn. and structure (measurements of Mie scattering, Raman scattering, scattering fluctuations, and of mass). The morphol. of the aerosol particles and the water uptake and drying behavior are investigated including the detn. of deliquescence and efflorescence relative humidities. In general, the thermodn. data derived from the measurements are in good agreement with previous work. The obsd. solid phase is mostly letovicite [(NH4)3H(SO4)2] and sometimes ammonium sulfate [(NH4)2SO4], whereas ammonium bisulfate [(NH4)HSO4] does not nucleate at temps. between 260 and 270 K despite supersatn. over periods of up to 1 day. This underlines the atm. importance of letovicite, which has been ignored in most previous studies concg. on ammonium sulfate. When the stoichiometry of the aq. soln. in the droplets is chosen as neither that of ammonium sulfate nor letovicite, the particles forming after efflorescence are mixed-phase particles (solid/liq.), representing the usual case in the natural atm. Upon crystn. these mixed-phase particles reveal a range of different morphologies with a tendency to form complex cryst. structures with embedded liq. cavities, but there is no evidence for the occurrence of cryst. material surrounded by the remaining liq. This liq. possibly resides in grain boundaries or triple junctions between single crystals or in small pores and shows little mobility upon extensive drying, unless the shell-like surrounding solid cracks.
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    34. 34
      Steimer, S. S.; Krieger, U. K.; Te, Y. F.; Lienhard, D. M.; Huisman, A. J.; Luo, B. P.; Ammann, M.; Peter, T. Electrodynamic Balance Measurements of Thermodynamic, Kinetic, and Optical Aerosol Properties Inaccessible to Bulk Methods. Atmos. Meas. Tech. 2015, 8, 2397– 2408,  DOI: 10.5194/amt-8-2397-2015
      There is no corresponding record for this reference.
    35. 35
      Davis, E. J.; Buehler, M. F.; Ward, T. L. The double-ring electrodynamic balance for microparticle characterization. Rev. Sci. Instrum. 1990, 61, 1281– 1288,  DOI: 10.1063/1.1141227
      35
      The double-ring electrodynamic balance for microparticle characterization
      Davis, E. James; Buehler, Mark F.; Ward, Timothy L.
      Review of Scientific Instruments (1990), 61 (4), 1281-8CODEN: RSINAK; ISSN:0034-6748.
      A simple form of the electrodynamic balance, suitable for a wide range of microparticle measurements, is described and analyzed. The a.c. electrode of the device consists of a pair of parallel rings, and the dc endcaps are either simple disks or they can be eliminated entirely by applying suitable d.c. bias voltages to the rings. The stability characteristics of the device are detd. by extension of well-established stability theory, and expts. are compared with that theory. The device is particularly well-suited for detection of radioactive aerosols, for it has significant advantages over the bihyperboloidal device for radioactivity measurement. The detection of radioactivity levels of <20 pCi is feasible. Coupled with a Raman spectrometer, the balance serves as a stable "platform" for the study of the chem. of microparticles, and both qual. and quant. anal. of microdroplet chem. are demonstrated for binary droplets of 1-octadecene and 1-bromoctadecane.
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    36. 36
      Zobrist, B.; Soonsin, V.; Luo, B. P.; Krieger, U. K.; Marcolli, C.; Peter, T.; Koop, T. Ultra-Slow Water Diffusion in Aqueous Sucrose Glasses. Phys. Chem. Chem. Phys. 2011, 13, 3514,  DOI: 10.1039/c0cp01273d
      36
      Ultra-slow water diffusion in aqueous sucrose glasses
      Zobrist, Bernhard; Soonsin, Vacharaporn; Luo, Bei P.; Krieger, Ulrich K.; Marcolli, Claudia; Peter, Thomas; Koop, Thomas
      Physical Chemistry Chemical Physics (2011), 13 (8), 3514-3526CODEN: PPCPFQ; ISSN:1463-9076. (Royal Society of Chemistry)
      We present measurements of water uptake and release by single micrometer-sized aq. sucrose particles. The expts. were performed in an electrodynamic balance where the particles can be stored contact-free in a temp. and humidity controlled chamber for several days. Aq. sucrose particles react to a change in ambient humidity by absorbing/desorbing water from the gas phase. This water absorption (desorption) results in an increasing (decreasing) droplet size and a decreasing (increasing) solute concn. Optical techniques were employed to follow minute changes of the droplet's size, with a sensitivity of 0.2 nm, as a result of changes in temp. or humidity. We exposed several particles either to humidity cycles (between ∼2% and 90%) at 291 K or to const. relative humidity and temp. conditions over long periods of time (up to several days) at temps. ranging from 203 to 291 K. In doing so, a retarded water uptake and release at low relative humidities and/or low temps. was obsd. Under the conditions studied here, the kinetics of this water absorption/desorption process is controlled entirely by liq.-phase diffusion of water mols. Hence, it is possible to derive the translational diffusion coeff. of water mols., DH2O, from these data by simulating the growth or shrinkage of a particle with a liq.-phase diffusion model. Values for DH2O-values as low as 10-24 m2 s-1 are detd. using data at temps. down to 203 K deep in the glassy state. From the expt. and modeling we can infer strong concn. gradients within a single particle including a glassy skin in the outer shells of the particle. Such glassy skins practically isolate the liq. core of a particle from the surrounding gas phase, resulting in extremely long equilibration times for such particles, caused by the strongly non-linear relationship between concn. and DH2O. We present a new parameterization of DH2O that facilitates describing the stability of aq. food and pharmaceutical formulations in the glassy state, the processing of amorphous aerosol particles in spray-drying technol., and the suppression of heterogeneous chem. reactions in glassy atm. aerosol particles.
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    37. 37
      Tang, I. N.; Munkelwitz, H. R. Water Activities, Densities, and Refractive Indices of Aqueous Sulfates and Sodium Nitrate Droplets of Atmospheric Importance. J. Geophys. Res.: Atmos. 1994, 99, 18801– 18808,  DOI: 10.1029/94jd01345
      There is no corresponding record for this reference.
    38. 38
      Zardini, A. A.; Sjogren, S.; Marcolli, C.; Krieger, U. K.; Gysel, M.; Weingartner, E.; Baltensperger, U.; Peter, T. A Combined Particle Trap/HTDMA Hygroscopicity Study of Mixed Inorganic/Organic Aerosol Particles. Atmos. Chem. Phys. 2008, 8, 5589– 5601,  DOI: 10.5194/acp-8-5589-2008
      38
      A combined particle trap/HTDMA hygroscopicity study of mixed inorganic/organic aerosol particles
      Zardini, A. A.; Sjogren, S.; Marcolli, C.; Krieger, U. K.; Gysel, M.; Weingartner, E.; Baltensperger, U.; Peter, T.
      Atmospheric Chemistry and Physics (2008), 8 (18), 5589-5601CODEN: ACPTCE; ISSN:1680-7316. (Copernicus Publications)
      Atm. aerosols are often mixts. of inorg. and org. material. Orgs. can represent a large fraction of the total aerosol mass and are comprised of water-sol. and insol. compds. Increasing attention was paid in the last decade to the capability of mixed inorg./org. aerosol particles to take up water (hygroscopicity). We performed hygroscopicity measurements of internally mixed particles contg. ammonium sulfate and carboxylic acids (citric, glutaric, adipic acid) in parallel with an electrodynamic balance (EDB) and a hygroscopicity tandem differential mobility analyzer (HTDMA). The org. compds. were chosen to represent three distinct phys. states. During hygroscopicity cycles covering hydration and dehydration measured by the EDB and the HTDMA, pure citric acid remained always liq., adipic acid remained always solid, while glutaric acid could be either. We show that the hygroscopicity of mixts. of the above compds. is well described by the Zdanovskii-Stokes-Robinson (ZSR) relationship as long as the two-component particle is completely liq. in the ammonium sulfate/glutaric acid system; deviations up to 10% in mass growth factor (corresponding to deviations up to 3.5% in size growth factor) are obsd. for the ammonium sulfate/citric acid 1:1 mixt. at 80% RH. We observe even more significant discrepancies compared to what is expected from bulk thermodn. when a solid component is present. We explain this in terms of a complex morphol. resulting from the crystn. process leading to veins, pores, and grain boundaries which allow for water sorption in excess of bulk thermodn. predictions caused by the inverse Kelvin effect on concave surfaces.
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    39. 39
      Chýlek, P. Partial-Wave Resonances and the Ripple Structure in the Mie Normalized Extinction Cross Section. J. Opt. Soc. Am. 1976, 66, 285– 287,  DOI: 10.1364/JOSA.66.000285
      There is no corresponding record for this reference.
    40. 40
      Bastelberger, S.; Krieger, U. K.; Luo, B.; Peter, T. Diffusivity Measurements of Volatile Organics in Levitated Viscous Aerosol Particles. Atmos. Chem. Phys. 2017, 17, 8453– 8471,  DOI: 10.5194/acp-17-8453-2017
      40
      Diffusivity measurements of volatile organics in levitated viscous aerosol particles
      Bastelberger, Sandra; Krieger, Ulrich K.; Luo, Beiping; Peter, Thomas
      Atmospheric Chemistry and Physics (2017), 17 (13), 8453-8471CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
      Field measurements indicating that atm. secondary org. aerosol (SOA) particles can be present in a highly viscous, glassy state have spurred numerous studies addressing low diffusivities of water in glassy aerosols. The focus of these studies is on kinetic limitations of hygroscopic growth and the plasticizing effect of water. In contrast, much less is known about diffusion limitations of org. mols. and oxidants in viscous matrixes. These may affect atm. chem. and gas-particle partitioning of complex mixts. with constituents of different volatility. In this study, we quantify the diffusivity of a volatile org. in a viscous matrix. Evapn. of single particles generated from an aq. soln. of sucrose and small amts. of volatile tetraethylene glycol (PEG-4) is investigated in an electrodynamic balance at controlled relative humidity (RH) and temp. The evaporative loss of PEG- 4 as detd. by Mie resonance spectroscopy is used in conjunction with a radially resolved diffusion model to retrieve translational diffusion coeffs. of PEG-4. Comparison of the exptl. derived diffusivities with viscosity ests. for the ternary system reveals a breakdown of the Stokes-Einstein relationship, which has often been invoked to infer diffusivity from viscosity. The evapn. of PEG-4 shows pronounced RH and temp. dependencies and is severely depressed for .ltorsim. 30 %, corresponding to diffusivities < 10-14 cm2 s-1 at temps. < 15 °C. The temp. dependence is strong, suggesting a diffusion activation energy of about 300 kJmol-1.We conclude that atm. volatile org. compds. can be subject to severe diffusion limitations in viscous org. aerosol particles. This may enable an important long-range transport mechanism for org. material, including pollutant mols. such as polycyclic arom. hydrocarbons (PAHs).
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    41. 41
      Dou, J.; Alpert, P. A.; Corral Arroyo, P.; Luo, B.; Schneider, F.; Xto, J.; Huthwelker, T.; Borca, C. N.; Henzler, K. D.; Raabe, J.; Watts, B.; Herrmann, H.; Peter, T.; Ammann, M.; Krieger, U. K. Photochemical Degradation of Iron(III) Citrate/Citric Acid Aerosol Quantified with the Combination of Three Complementary Experimental Techniques and a Kinetic Process Model. Atmos. Chem. Phys. 2021, 21, 315– 338,  DOI: 10.5194/acp-21-315-2021
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      Photochemical degradation of iron(III) citrate/citric acid aerosol quantified with the combination of three complementary experimental techniques and a kinetic process model
      Dou, Jing; Alpert, Peter A.; Arroyo, Pablo Corral; Luo, Beiping; Schneider, Frederic; Xto, Jacinta; Huthwelker, Thomas; Borca, Camelia N.; Henzler, Katja D.; Raabe, Jorg; Watts, Benjamin; Herrmann, Hartmut; Peter, Thomas; Ammann, Markus; Krieger, Ulrich K.
      Atmospheric Chemistry and Physics (2021), 21 (1), 315-338CODEN: ACPTCE; ISSN:1680-7324. (Copernicus Publications)
      Iron(III) carboxylate photochem. plays an important role in aerosol aging, esp. in the lower troposphere. These complexes can absorb light over a broad wavelength range, inducing the redn. of iron(III) and the oxidn. of carboxylate ligands. In the presence of O2, the ensuing radical chem. leads to further decarboxylation, and the prodn. of ·OH, HO·2, peroxides, and oxygenated volatile org. compds., contributing to particle mass loss. The ·OH, HO·2, and peroxides in turn reoxidize iron(II) back to iron(III), closing a photocatalytic cycle. This cycle is repeated, resulting in continual mass loss due to the release of CO2 and other volatile compds. In a cold and/or dry atm., org. aerosol particles tend to attain highly viscous states. While the impact of reduced mobility of aerosol constituents on dark chem. reactions has received substantial attention, studies on the effect of high viscosity on photochem. processes are scarce. Here, we choose iron(III) citrate (FeIII(Cit)) as a model light-absorbing iron carboxylate complex that induces citric acid (CA) degrdn. to investigate how transport limitations influence photochem. processes. Three complementary exptl. approaches were used to investigate kinetic transport limitations. The mass loss of single, levitated particles was measured with an electrodynamic balance, the oxidn. state of deposited particles was measured with X-ray spectromicroscopy, and HO·2 radical prodn. and release into the gas phase was obsd. in coated-wall flow-tube expts. We obsd. significant photochem. degrdn. with up to 80 ‰ mass loss within 24 h of light exposure. Interestingly, we also obsd. that mass loss always accelerated during irradn., resulting in an increase of the mass loss rate by about a factor of 10. When we increased relative humidity (RH), the obsd. particle mass loss rate also increased. This is consistent with strong kinetic transport limitations for highly viscous particles. To quant. compare these expts. and det. important phys. and chem. parameters, a numerical multilayered photochem. reaction and diffusion (PRAD) model was developed that treats chem. reactions and the transport of various species. The PRAD model was tuned to simultaneously reproduce all exptl. results as closely as possible and captured the essential chem. and transport during irradn. In particular, the photolysis rate of FeIII, the reoxidn. rate of FeII, HO·2 prodn., and the diffusivity of O2 in aq. FeIII(Cit) / CA system as function of RH and FeIII(Cit) / CA molar ratio could be constrained. This led to satisfactory agreement within model uncertainty for most but not all expts. performed. Photochem. degrdn. under atm. conditions predicted by the PRAD model shows that release of CO2 and repartitioning of org. compds. to the gas phase may be very important when attempting to accurately predict org. aerosol aging processes.
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    42. 42
      Carslaw, K. S.; Clegg, S. L.; Brimblecombe, P. A Thermodynamic Model of the System HCl-HNO3-H2SO4-H2O, Including Solubilities of HBr, from <200 to 328 K. J. Phys. Chem. 1995, 99, 11557– 11574,  DOI: 10.1021/j100029a039
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      A Thermodynamic Model of the System HCl-HNO3-H2SO4-H2O, Including Solubilities of HBr, from <200 to 328 K
      Carslaw, Kenneth S.; Clegg, Simon L.; Brimblecombe, Peter
      Journal of Physical Chemistry (1995), 99 (29), 11557-74CODEN: JPCHAX; ISSN:0022-3654.
      A multicomponent mole-fraction-based thermodn. model, together with Henry's law consts. and the vapor pressure of pure water, was used to represent aq. phase activities, vapor pressures (of H2O, HNO3, HCl, and HBr), and satn. with respect to solid phases (ice, H2SO4·nH2O, HNO3·nH2O, and HCl·3H2O) in the system HCl-HBr-HNO3-H2SO4-H2O. The model is valid from 330 to <200 K, and up to ∼40 mol/kg total solute molality for solns. contg. mainly H2SO4 and HNO3. Model parameters for pure aq. H2SO4 were adopted from a previous study, and values for HNO3-H2O, HCl-H2O, and HBr-H2O were obtained by fitting to activity and osmotic coeffs., emf. (emf) measurements, vapor pressures, f. ps., and thermal (enthalpy and heat capacity) data. The model was tested by using measured partial pressures and solubilities of HCl in aq. H2SO4 from 330 to 200 K, HBr solubilities in aq. H2SO4 from ∼240 to 205 K, and HNO3 partial pressures and f. ps. for HNO3-H2SO4-H2O mixts. from 273.15 to <200 K. Ternary (mixt.) parameters were required only for HNO3-H2SO4-H2O. Solubilities of HNO3, HCl, and HBr in liq. stratospheric aerosols are calcd.
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    43. 43
      Luo, B.; Carslaw, K. S.; Peter, T.; Clegg, S. L. Vapour Pressures of H2SO4/HNO3/HCl/HBr/H2O Solutions to Low Stratospheric Temperatures. Geophys. Res. Lett. 1995, 22, 247– 250,  DOI: 10.1029/94GL02988
      43
      Vapor pressures of H2SO4/HNO3/HCl/HBr/H2O solutions to low stratospheric temperatures
      Luo, Beiping; Carslaw, Kenneth S.; Peter, Thomas; Clegg, Simon L.
      Geophysical Research Letters (1995), 22 (3), 247-50CODEN: GPRLAJ; ISSN:0094-8276.
      Vapor pressures of H2O, HNO3, HCl and HBr over supercooled aq. mixts. with sulfuric acid have been calcd. using an activity coeff. model, for 185 K < T < 235 K, 0 < wt.% (H2SO4) + wt.%(HNO3) < 70, and assuming HCl and HBr to be minor constituents. Predicted vapor pressures agree well with most lab. data, and give confidence in the validity of the model. The results are parameterized as simple formulas, which reproduce the model results to within 40% and cover the entire stratospherically relevant range of compn. and temp.
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    44. 44
      Lin, K.; Schulte, C. R.; Marr, L. C. Survival of MS2 and Φ6 viruses in droplets as a function of relative humidity, pH, and salt, protein, and surfactant concentrations. PLoS One 2020, 15, e0243505  DOI: 10.1371/journal.pone.0243505
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      Survival of MS2 and Φ6 viruses in droplets as a function of relative humidity, pH, and salt, protein, and surfactant concentrations
      Lin, Kaisen; Schulte, Chase R.; Marr, Linsey C.
      PLoS One (2020), 15 (12), e0243505CODEN: POLNCL; ISSN:1932-6203. (Public Library of Science)
      The survival of viruses in droplets is known to depend on droplets' chem. compn., which may vary in respiratory fluid between individuals and over the course of disease. This relationship is also important for understanding the persistence of viruses in droplets generated from wastewater, freshwater, and seawater. We investigated the effects of salt (0, 1, and 35 g/L), protein (0, 100, and 1000μg/mL), surfactant (0, 1, and 10μg/mL), and droplet pH (4.0, 7.0, and 10.0) on the viability of viruses in 1-μL droplets pipetted onto polystyrene surfaces and exposed to 20%, 50%, and 80% relative humidity (RH) using a culture-based approach. Results showed that viability of MS2, a non-enveloped virus, was generally higher than that of Φ6, an enveloped virus, in droplets after 1 h. The chem. compn. of droplets greatly influenced virus viability. Specifically, the survival of MS2 was similar in droplets at different pH values, but the viability of Φ6 was significantly reduced in acidic and basic droplets compared to neutral ones. The presence of bovine serum albumin protected both MS2 and Φ6 from inactivation in droplets. The effects of sodium chloride and the surfactant sodium dodecyl sulfate varied by virus type and RH. Meanwhile, RH affected the viability of viruses as shown previously: viability was lowest at intermediate to high RH. The results demonstrate that the viability of viruses is detd. by the chem. compn. of carrier droplets, esp. pH and protein content, and environmental factors. These findings emphasize the importance of understanding the chem. compn. of carrier droplets in order to predict the persistence of viruses contained in them.
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    45. 45
      Galloway, S. E.; Reed, M. L.; Russell, C. J.; Steinhauer, D. A. Influenza HA Subtypes Demonstrate Divergent Phenotypes for Cleavage Activation and PH of Fusion: Implications for Host Range and Adaptation. PLoS Pathog. 2013, 9, e1003151  DOI: 10.1371/journal.ppat.1003151
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      Influenza HA subtypes demonstrate divergent phenotypes for cleavage activation and pH of fusion: implications for host range and adaptation
      Galloway, Summer E.; Reed, Mark L.; Russell, Charles J.; Steinhauer, David A.
      PLoS Pathogens (2013), 9 (2), e1003151CODEN: PPLACN; ISSN:1553-7374. (Public Library of Science)
      The influenza A virus (IAV) HA protein must be activated by host cells proteases in order to prime the mol. for fusion. Consequently, the availability of activating proteases and the susceptibility of HA to protease activity represents key factors in facilitating virus infection. As such, understanding the intricacies of HA cleavage by various proteases is necessary to derive insights into the emergence of pandemic viruses. To examine these properties, we generated a panel of HAs that are representative of the 16 HA subtypes that circulate in aquatic birds, as well as HAs representative of the subtypes that have infected the human population over the last century. We examd. the susceptibility of the panel of HA proteins to trypsin, as well as human airway trypsin-like protease (HAT) and transmembrane protease, serine 2 (TMPRSS2). Addnl., we examd. the pH at which these HAs mediated membrane fusion, as this property is related to the stability of the HA mol. and influences the capacity of influenza viruses to remain infectious in natural environments. Our results show that cleavage efficiency can vary significantly for individual HAs, depending on the protease, and that some HA subtypes display stringent selectivity for specific proteases as activators of fusion function. Addnl., we found that the pH of fusion varies by 0.7 pH units among the subtypes, and notably, we obsd. that the pH of fusion for most HAs from human isolates was lower than that obsd. from avian isolates of the same subtype. Overall, these data provide the first broad-spectrum anal. of cleavage-activation and membrane fusion characteristics for all of the IAV HA subtypes, and also show that there are substantial differences between the subtypes that may influence transmission among hosts and establishment in new species.
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    46. 46
      Bullough, P. A.; Hughson, F. M.; Skehel, J. J.; Wiley, D. C. Structure of Influenza Haemagglutinin at the PH of Membrane Fusion. Nature 1994, 371, 37– 43,  DOI: 10.1038/371037a0
      45
      Structure of influenza hemagglutinin at the pH of membrane fusion
      Bullough, Per A.; Hughson, Frederick M.; Skehel, John J.; Wiley, Don C.
      Nature (London, United Kingdom) (1994), 371 (6492), 37-43CODEN: NATUAS; ISSN:0028-0836.
      Low pH induces a conformational change in the influenza virus hemagglutinin, which then mediates fusion of the viral and host cell membranes. The three-dimensional structure of a fragment of the hemagglutinin in this conformation reveals a major refolding of the secondary and tertiary structure of the mol. The apolar fusion peptide moves at least 100 Å to one tip of the mol. At the other end a helical segment unfolds, a subdomain relocates reversing the chain direction, and part of the structure becomes disordered.
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    47. 47
      Jackson, C. B.; Farzan, M.; Chen, B.; Choe, H. Mechanisms of SARS-CoV-2 Entry into Cells. Nat. Rev. Mol. Cell Biol. 2022, 23, 3– 20,  DOI: 10.1038/s41580-021-00418-x
      46
      Mechanisms of SARS-CoV-2 entry into cells
      Jackson, Cody B.; Farzan, Michael; Chen, Bing; Choe, Hyeryun
      Nature Reviews Molecular Cell Biology (2022), 23 (1), 3-20CODEN: NRMCBP; ISSN:1471-0072. (Nature Portfolio)
      A review. The unprecedented public health and economic impact of the COVID-19 pandemic caused by infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been met with an equally unprecedented scientific response. Much of this response has focused, appropriately, on the mechanisms of SARS-CoV-2 entry into host cells, and in particular the binding of the spike (S) protein to its receptor, angiotensin-converting enzyme 2 (ACE2), and subsequent membrane fusion. This Review provides the structural and cellular foundations for understanding the multistep SARS-CoV-2 entry process, including S protein synthesis, S protein structure, conformational transitions necessary for assocn. of the S protein with ACE2, engagement of the receptor-binding domain of the S protein with ACE2, proteolytic activation of the S protein, endocytosis and membrane fusion. We define the roles of furin-like proteases, transmembrane protease, serine 2 (TMPRSS2) and cathepsin L in these processes, and delineate the features of ACE2 orthologues in reservoir animal species and S protein adaptations that facilitate efficient human transmission. We also examine the utility of vaccines, antibodies and other potential therapeutics targeting SARS-CoV-2 entry mechanisms. Finally, we present key outstanding questions assocd. with this crit. process.
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    48. 48
      Huynh, E.; Olinger, A.; Woolley, D.; Kohli, R. K.; Choczynski, J. M.; Davies, J. F.; Lin, K.; Marr, L. C.; Davis, R. D. Evidence for a Semisolid Phase State of Aerosols and Droplets Relevant to the Airborne and Surface Survival of Pathogens. Proc. Natl. Acad. Sci. U.S.A. 2022, 119, e2109750119  DOI: 10.1073/pnas.2109750119
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      Evidence for a semisolid phase state of aerosols and droplets relevant to the airborne and surface survival of pathogens
      Huynh, Erik; Olinger, Anna; Woolley, David; Kohli, Ravleen Kaur; Choczynski, Jack M.; Davies, James F.; Lin, Kaisen; Marr, Linsey C.; Davis, Ryan D.
      Proceedings of the National Academy of Sciences of the United States of America (2022), 119 (4), e2109750119CODEN: PNASA6; ISSN:0027-8424. (National Academy of Sciences)
      The phase state of respiratory aerosols and droplets has been linked to the humidity-dependent survival of pathogens such as SARS-CoV-2. To inform strategies to mitigate the spread of infectious disease, it is thus necessary to understand the humidity-dependent phase changes assocd. with the particles in which pathogens are suspended. Here, we study phase changes of levitated aerosols and droplets composed of model respiratory compds. (salt and protein) and growth media (org.-inorg. mixts. commonly used in studies of pathogen survival) with decreasing relative humidity (RH). Efflorescence was suppressed in many particle compns. and thus unlikely to fully account for the humidity-dependent survival of viruses. Rather, we identify org.-based, semisolid phase states that form under equil. conditions at intermediate RH (45 to 80%). A higher-protein content causes particles to exist in a semisolid state under a wider range of RH conditions. Diffusion and, thus, disinfection kinetics are expected to be inhibited in these semisolid states. These observations suggest that org.-based, semisolid states are an important consideration to account for the recovery of virus viability at low RH obsd. in previous studies. We propose a mechanism in which the semisolid phase shields pathogens from inactivation by hindering the diffusion of solutes. This suggests that the exogenous lifetime of pathogens will depend, in part, on the org. compn. of the carrier respiratory particle and thus its origin in the respiratory tract. Furthermore, this work highlights the importance of accounting for spatial heterogeneities and time-dependent changes in the properties of aerosols and droplets undergoing evapn. in studies of pathogen viability.
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    49. 49
      Klein, L. K.; Luo, B.; Bluvshtein, N.; Krieger, U. K.; Schaub, A.; Glas, I.; David, S. C.; Violaki, K.; Motos, G.; Pohl, M. O.; Hugentobler, W.; Nenes, A.; Stertz, S.; Peter, T.; Kohn, T. Expiratory Aerosol PH Is Determined by Indoor Room Trace Gases and Particle Size. Proc. Natl. Acad. Sci. U.S.A. 2022, 119, e2212140119  DOI: 10.1073/pnas.2212140119
      There is no corresponding record for this reference.
    50. 50
      The National Institute for Occupational Safety and Health (NIOSH). CDC─NIOSH Pocket Guide to Chemical Hazards─Nitric acid. Time-Weighted Average (TWA) of the Permissible Exposure Limit (PEL), Legal 8-hour Limit in the United States for Exposure of an Employee 2 ppm for HNO3. https://www.cdc.gov/niosh/npg/npgd0447.html (accessed Nov 2, 2022).
      There is no corresponding record for this reference.
    51. 51
      German Social Accident Insurance (DGUV). GESTIS International Limit Values. National Occupational Exposure Limits (OELs) in the European Union, Legal 8 h Limit, 0.5–2 ppm for HNO3, Depending on Country. https://limitvalue.ifa.dguv.de/WebForm_ueliste2.aspx (accessed Nov 2, 2022).
      There is no corresponding record for this reference.
    52. 52
      Nicola, A. V.; McEvoy, A. M.; Straus, S. E. Roles for Endocytosis and Low PH in Herpes Simplex Virus Entry into HeLa and Chinese Hamster Ovary Cells. J. Virol. 2003, 77, 5324– 5332,  DOI: 10.1128/JVI.77.9.5324-5332.2003
      51
      Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells
      Nicola, Anthony V.; McEvoy, Anna M.; Straus, Stephen E.
      Journal of Virology (2003), 77 (9), 5324-5332CODEN: JOVIAM; ISSN:0022-538X. (American Society for Microbiology)
      Herpes simplex virus (HSV) infection of many cultured cells, e.g., Vero cells, can be initiated by receptor binding and pH-neutral fusion with the cell surface. Here we report that a major pathway for HSV entry into the HeLa and CHO-K1 cell lines is dependent on endocytosis and exposure to a low pH. Enveloped virions were readily detected in HeLa or receptor-expressing CHO cell vesicles by electron microscopy at <30 min postinfection. As expected, images of virus fusion with the Vero cell surface were prevalent. Treatment with energy depletion or hypertonic medium, which inhibits endocytosis, prevented uptake of HSV from the HeLa and CHO cell surface relative to uptake from the Vero cell surface. Incubation of HeLa and CHO cells with the weak base ammonium chloride or the ionophore monensin, which elevate the low pH of organelles, blocked HSV entry in a dose-dependent manner. Noncytotoxic concns. of these agents acted at an early step during infection by HSV type 1 and 2 strains. Entry mediated by the HSV receptor HveA, nectin-1, or nectin-2 was also blocked. As analyzed by fluorescence microscopy, lysosomotropic agents such as the vacuolar H+-ATPase inhibitor bafilomycin A1 blocked the delivery of virus capsids to the nuclei of the HeLa and CHO cell lines but had no effect on capsid transport in Vero cells. The results suggest that HSV can utilize two distinct entry pathways, depending on the type of cell encountered.
      >> More from SciFinder ®
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    53. 53
      Ausar, S. F.; Rexroad, J.; Frolov, V. G.; Look, J. L.; Konar, N.; Middaugh, C. R. Analysis of the Thermal and PH Stability of Human Respiratory Syncytial Virus. Mol. Pharm. 2005, 2, 491– 499,  DOI: 10.1021/mp0500465
      52
      Analysis of the Thermal and pH Stability of Human Respiratory Syncytial Virus
      Ausar, Salvador F.; Rexroad, Jason; Frolov, Vladimir G.; Look, Jee L.; Konar, Nandini; Middaugh, C. Russell
      Molecular Pharmaceutics (2005), 2 (6), 491-499CODEN: MPOHBP; ISSN:1543-8384. (American Chemical Society)
      Respiratory syncytial virus (RSV) was studied as a function of pH (3-8) and temp. (10-85°) by fluorescence, CD, and high-resoln. second-deriv. absorbance spectroscopies, as well as dynamic light scattering and optical d. as a measurement of viral aggregation. The results indicate that the secondary, tertiary, and quaternary structures of RSV are both pH and temp. labile. Deriv. UV absorbance and fluorescence spectroscopy (intrinsic and extrinsic) analyses suggest that the stability of tertiary structure of RSV proteins is maximized near neutral pH. In agreement with these results, the secondary structure of RSV polypeptides seems to be more stable at pH 7-8, as evaluated by CD spectroscopy. The integrity of the viral particles studied by turbidity and dynamic light scattering also revealed that RSV is more thermally stable near neutral pH and particularly prone to aggregation below pH 6. By combination of the spectroscopic data employing a multidimensional eigenvector phase space approach, an empirical phase diagram for RSV was constructed. The pharmaceutical utility of this approach and the optimal formulation conditions are discussed.
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      Darnell, M. E. R.; Subbarao, K.; Feinstone, S. M.; Taylor, D. R. Inactivation of the Coronavirus That Induces Severe Acute Respiratory Syndrome, SARS-CoV. J. Virol. Methods 2004, 121, 85– 91,  DOI: 10.1016/j.jviromet.2004.06.006
      53
      Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV
      Darnell, Miriam E. R.; Subbarao, Kanta; Feinstone, Stephen M.; Taylor, Deborah R.
      Journal of Virological Methods (2004), 121 (1), 85-91CODEN: JVMEDH; ISSN:0166-0934. (Elsevier B.V.)
      Severe acute respiratory syndrome (SARS) is a life-threatening disease caused by a novel coronavirus termed SARS-CoV. Due to the severity of this disease, the World Health Organization (WHO) recommends that manipulation of active viral cultures of SARS-CoV be performed in containment labs. at biosafety level 3 (BSL3). The virus was inactivated by UV light (UV) at 254 nm, heat treatment of 65 or greater, alk. (pH > 12) or acidic (pH < 3) conditions, formalin and glutaraldehyde treatments. We describe the kinetics of these efficient viral inactivation methods, which will allow research with SARS-CoV contg. materials, that are rendered non-infectious, to be conducted at reduced safety levels.
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      https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADC%252BD2cXntlSls7s%253D&md5=317883b050d5248b339edeccf3377267
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      Seinfeld, J. H.; Pandis, S. N. Atmospheric Chemistry and Physics: From Air Pollution to Climate Change, 6th ed.; Wiley: Hoboken, NJ, 2006.
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      Neuman, J. A.; Huey, L. G.; Ryerson, T. B.; Fahey, D. W. Study of Inlet Materials for Sampling Atmospheric Nitric Acid. Environ. Sci. Technol. 1999, 33, 1133– 1136,  DOI: 10.1021/es980767f
      55
      Study of Inlet Materials for Sampling Atmospheric Nitric Acid
      Neuman, J. A.; Huey, L. G.; Ryerson, T. B.; Fahey, D. W.
      Environmental Science and Technology (1999), 33 (7), 1133-1136CODEN: ESTHAG; ISSN:0013-936X. (American Chemical Society)
      The adsorption of nitric acid from a flowing gas stream is studied for a variety of wall materials to det. their suitability for use in atm. sampling instruments. Ppb level mixts. of HNO3 in synthetic air flow through tubes of different materials in such a way that >80% of the mols. interact with the walls. A chem. ionization mass spectrometer with a fast time response and high sensitivity detects HNO3 that is not adsorbed on the tube walls. Less than 5% of available HNO3 is adsorbed on Teflon fluoropolymer tubing after 1 min of HNO3 exposure, whereas >70% is lost on walls made of stainless steel, glass, fused silica, aluminum, nylon, silica-steel, and silane-coated glass. Glass tubes exposed to HNO3 on the order of hours passivate with HNO3 adsorption dropping to zero. The adsorption of HNO3 on PFA Teflon tubing (PFA) is nearly temp.-independent from 10 to 80°, but below -10° nearly all HNO3 that interacts with PFA is reversibly adsorbed. In ambient and synthetic air, humidity increases HNO3 adsorption. The results suggest that Teflon at temps. above 10° is an optimal choice for inlet surfaces used for in situ measurements of HNO3 in the ambient atm.
      >> More from SciFinder ®
      https://chemport.cas.org/services/resolver?origin=ACS&resolution=options&coi=1%3ACAS%3A528%3ADyaK1MXhtVOlsrY%253D&md5=0b77b1007a0ce3abad5867916426b396
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      Pöhlker, M. L.; Krüger, O. O.; Förster, J.-D.; Berkemeier, T.; Elbert, W.; Fröhlich-Nowoisky, J.; Pöschl, U.; Pöhlker, C.; Bagheri, G.; Bodenschatz, E.; Huffman, J. A.; Scheithauer, S.; Mikhailov, E. Respiratory Aerosols and Droplets in the Transmission of Infectious Diseases, 2021. arXiv:210301188. arXiv Prepr. https://doi.org/10.48550/arXiv.2103.01188.
      There is no corresponding record for this reference.

  • Supporting Information

    Supporting Information

    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.2c05777.

    • Method descriptions for virus and matrix preparation, measurement of viral aggregates and electron microscopy for SLF characterization; further details for EDB measurements; in-depth description of ResAM, its uncertainties, and limitations; descriptive comparison of ResAM results with published data; investigation of acetic acid as a potential agent against airborne viruses; particle-shell model; extent and effect of virus aggregation at low pH and high ionic strength; exemplary inactivation curves; additional EDB measurements; (electron) microscopy images of SLF; evolution of physicochemical conditions within aerosols at 80% RH; modeled inactivation times in the presence of acetic acid; modeled inactivation times of HCoV-229E; ResAM sensitivity study results; visual comparison of literature inactivation data and ResAM results; viral load and transmission risk for breathing, coughing, and singing at different air compositions and ventilation rates; substantiation of the assumptions of the ResAM model; composition of SLF; equilibrium constants; liquid-phase diffusion coefficients; and air compositions used in the ResAM model (PDF)


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