Humidity-Dependent Survival of an Airborne Influenza A Virus: Practical Implications for Controlling Airborne Viruses

Abstract

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 determined 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 superdeliquescence zone air, yielding aerosols in the effloresced or noneffloresced state, respectively. We then adjusted the RH to an ergonomically comfortable RH (60%). Fifteen minutes post-aerosolization, the surviving fractions (arithmetic means ± standard 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% saturated RH to these zonal ranges. Fifteen minutes post-aerosolization, the surviving fractions were 3 ± 0.4%, 2 ± 0.1%, and 12 ± 2%, respectively. 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.

Drying of virus-containing particles: modelling effects of droplet origin and composition

“…For some viruses inactivation is faster at intermediate levels of relative humidity, around 40-60%, than at high or very low humidity [20]. This pattern was observed in two recent studies, on the non-enveloped common cold virus HRV-16 [21] and on influenza virus A, an enveloped virus [22]. In both studies the virus was inactivated faster at 60% RH when it had been dried from higher RH than when it had been hydrated from lower RH [21,22].…”

“…This pattern was observed in two recent studies, on the non-enveloped common cold virus HRV-16 [21] and on influenza virus A, an enveloped virus [22]. In both studies the virus was inactivated faster at 60% RH when it had been dried from higher RH than when it had been hydrated from lower RH [21,22]. This observation was explained as follows, based on an "Efflorescence-deliquescence differential inactivation" model.…”

“…Realworld aerosol droplets [25] are therefore likely to show less extreme behaviour than simple salt mixtures. While model airway fluids [22,29] showed clear efflorescence-deliquescence hysteresis, hysteresis was variable in cough aerosols from different individuals and was not evident in aerosols from some subjects [25].…”

“…In artificial media, in both aerosol form [20][21][22] and as surface deposits [29], several viruses are inactivated faster in the intermediate RH region where hysteresis is observed, compared with low or high RH. Suggested mechanisms include the direct effect of elevated salt concentration [29]; the removal of structural water [20]; the disruption of hydrophobic bonding at low water activity [30] and changes in pH [20,70].…”

“…In the hysteresis region between the efflorescence and deliquescence limits (typically about 35% to 65% RH) [25], the salt concentration can rise considerably above that predicted from equilibrium solubility. It was suggested [21,22] that high salt concentration inactivated the HRV-16 and IVA viruses.…”