Ambient carbon dioxide concentration correlates with SARS-CoV-2 aerostability and infection risk
Allen Haddrell, Henry Oswin, Mara Otero-Fernandez, Joshua F Robinson, Tristan Cogan, Robert Alexander, Jamie F S Mann, Darryl Hill, Adam Finn, Andrew D Davidson, Jonathan P Reid
Nature Communications, doi:10.1038/s41467-024-47777-5
An improved understanding of the underlying physicochemical properties of respiratory aerosol that influence viral infectivity may open new avenues to mitigate the transmission of respiratory diseases such as COVID-19. Previous studies have shown that an increase in the pH of respiratory aerosols following generation due to changes in the gas-particle partitioning of pH buffering bicarbonate ions and carbon dioxide is a significant factor in reducing SARS-CoV-2 infectivity. We show here that a significant increase in SARS-CoV-2 aerostability results from a moderate increase in the atmospheric carbon dioxide concentration (e.g. 800 ppm), an effect that is more marked than that observed for changes in relative humidity. We model the likelihood of COVID-19 transmission on the ambient concentration of CO 2 , concluding that even this moderate increase in CO 2 concentration results in a significant increase in overall risk. These observations confirm the critical importance of ventilation and maintaining low CO 2 concentrations in indoor environments for mitigating disease transmission. Moreover, the correlation of increased CO 2 concentration with viral aerostability need to be better understood when considering the consequences of increases in ambient CO 2 levels in our atmosphere. The inhalation of respiratory aerosol containing the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) has been identified as an important route of transmission in the spread of coronavirus disease 2019 (COVID-19) 1 . As for all respiratory viral infections, a sufficient viral dose must be delivered to the respiratory system of an uninfected individual for disease transmission to occur. For COVID-19, this equates to inhalation of a sufficient quantity of aerosolized/ inhalable and infectious SARS-CoV-2 viral particles. The minimal infectious dose is a function of many parameters, such as mucosal immunity 2 , prior infection 3 , and immunization status 4 . Regardless of the infectious dose required, the cumulative viral load of the air inhaled will necessarily correlate with the overall risk. Thus, understanding how environmental factors affect the aerosolized viral load over time will contribute to the assessment of the risk of transmission. At their core, many of the non-pharmaceutical interventions implemented to mitigate the risk of COVID-19 transmission are centered on the removal of infectious aerosolized virus from a given space. The aerosolized viral load may be altered physically by lowering
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Author contributions
Competing interests The authors declare no competing interests.
Additional information
Supplementary information The online version contains supplementary material available at https://doi.org/10.1038/s41467-024-47777-5. Correspondence and requests for materials should be addressed to Allen Haddrell, Andrew D. Davidson or Jonathan P. Reid. Peer review information Nature Communications thanks the anonymous reviewer(s) for their contribution to the peer review of this work. A peer review file is available. Reprints and permissions information is available at http://www.nature.com/reprints Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence..
References
Alexander, Mucin transiently sustains coronavirus infectivity through heterogenous changes in phase morphology of evaporating aerosol, Viruses
Archer, Comparing aerosol number and mass exhalation rates from children and adults during breathing, speaking and singing, Interface Focus,
doi:10.1098/rsfs.2021.0078
Bardow, Madsen, Nauntofte, The bicarbonate concentration in human saliva does not exceed the plasma level under normal physiological conditions, Clin. Oral. Investig
Batéjat, Grassin, Manuguerra, Leclercq, Heat inactivation of the severe acute respiratory syndrome coronavirus 2, J. Biosaf. Biosecur
Bobrovitz, Protective effectiveness of previous SARS-CoV-2 infection and hybrid immunity against the omicron variant and severe disease: a systematic review and meta-regression, Lancet Infect. Dis
Bogdanovica, Zemitis, Bogdanovics, The effect of CO2 concentration on children's well-being during the process of learning, Energies
Bushmaker, Comparative aerosol and surface stability of SARS-CoV-2 variants of concern, Emerg. Infect. Dis
Cheng, Global monthly gridded atmospheric carbon dioxide concentrations under the historical and future scenarios, Sci. Data
Chiu, Chen, Chang, Carbon dioxide concentrations and temperatures within tour buses under real-time traffic conditions, PLoS ONE
Cobb, Fast CO2 hydration kinetics impair heterogeneous but improve enzymatic CO2 reduction catalysis, Nat. Chem
Dabisch, The influence of temperature, humidity, and simulated sunlight on the infectivity of SARS-CoV-2 in aerosols, Aerosol Sci. Tech
Deng, Lau, Seasonal variations of indoor air quality and thermal conditions and their correlations in 220 classrooms in the Midwestern United States, Build Environ
Di Gilio, CO2 concentration monitoring inside educational buildings as a strategic tool to reduce the risk of Sars-CoV-2 airborne transmission, Environ. Res,
doi:10.1016/j.envres.2021.111560
Downing, Computational and experimental study of aerosol dispersion in a ventilated room, Aerosol Sci. Tech
Duval, Long distance airborne transmission of SARS-CoV-2: rapid systematic review, BMJ
Elbayoumi, Ramli, Md Yusof, Madhoun, The effect of seasonal variation on indoor and outdoor carbon monoxide concentrations in Eastern Mediterranean climate, Atmos. Pollut. Res
Fears, Persistence of severe acute respiratory syndrome coronavirus 2 in aerosol suspensions, Emerg. Infect. Dis
Fernandez, Assessing the airborne survival of bacteria in populations of aerosol droplets with a novel technology, J. R. Soc. Interface
Fernandez, Thomas, Oswin, Haddrell, Reid, Transformative approach to investigate the microphysical factors influencing airborne transmission of pathogens, Appl. Environ. Micro
Foglio Bonda, Pattarino, Foglio-Bonda, Kinematic viscosity of unstimulated whole saliva in healthy young adults, Eur. Rev. Med. Pharmacol. Sci
Glogowsky, Hansen, Schächtele, How effective are social distancing policies? Evidence on the fight against COVID-19, PLoS ONE
Gregson, Comparing aerosol concentrations and particle size distributions generated by singing, speaking and breathing, Aerosol Sci. Tech
Haddrell, Differences in airborne stability of SARS-CoV-2 variants of concern is impacted by alkalinity of surrogates of respiratory aerosol, J. R. Soc. Interface
Herstein, Characteristics of SARS-CoV-2 transmission among meat processing workers in Nebraska, USA, and effectiveness of risk mitigation measures, Emerg. Infect. Dis
Kostikas, pH in expired breath condensate of patients with inflammatory airway diseases, Am. J. Resp. Crit. Care
Kudo, Low ambient humidity impairs barrier function and innate resistance against influenza infection, Proc. Natl Acad. Sci
Leech, Mask wearing in community settings reduces SARS-CoV-2 transmission, Proc. Natl Acad. Sci. USA
Li, Airborne dispersion of droplets during coughing: a physical model of viral transmission, Sci. Rep
Lipinski, Ahmad, Serey, Jouhara, Review of ventilation strategies to reduce the risk of disease transmission in high occupancy buildings, Int. J. Thermofluids
Lowen, Steel, Roles of humidity and temperature in shaping influenza seasonality, J. Virol
Majra, Benson, Pitts, Stebbing, SARS-CoV-2 (COVID-19) superspreader events, J. Infect
Moriyama, Hugentobler, Iwasaki, Seasonality of respiratory viral infections, Annu. Rev. Virol
Nissen, Long-distance airborne dispersal of SARS-CoV-2 in COVID-19 wards, Sci. Rep
Oswin, Measuring stability of virus in aerosols under varying environmental conditions, Aerosol Sci. Tech
Oswin, The dynamics of SARS-CoV-2 infectivity with changes in aerosol microenvironment, Proc. Natl Acad. Sci
Oswin, the importance of aerosol pH for airborne respiratory virus transmission, Proc. Natl Acad. Sci. USA
Park, Effects of temperature, humidity, and diurnal temperature range on influenza incidence in a temperate region, Influenza Other Respir. Viruses
Peng, Jimenez, Exhaled CO(2) as a COVID-19 infection risk proxy for different indoor, Environ. Sci. Technol. Lett
Riley, Murphy, Riley, Airborne spread of measles in a suburban elementary school, Am. J. Epidemiol
Rosias, Childhood asthma: exhaled markers of airway inflammation, asthma control score, and lung function tests, Pediatr. Pulmonol
Russell, Moldoveanu, Ogra, Mestecky, Mucosal immunity in COVID-19: a neglected but critical aspect of SARS-CoV-2 infection, Front. Immunol
Schuit, Airborne SARS-CoV-2 is rapidly inactivated by simulated sunlight, J. Infect. Dis
Smither, Eastaugh, Findlay, Lever, Experimental aerosol survival of SARS-CoV-2 in artificial saliva and tissue culture media at medium and high humidity, Emerg. Microbes Infect
Tanisali, Effectiveness of different types of mask in aerosol dispersion in SARS-CoV-2 infection, Int. J. Infect. Dis
Team, Past SARS-CoV-2 infection protection against re-infection: a systematic review and meta-analysis, Lancet
Thornton, The impact of heating, ventilation, and air conditioning design features on the transmission of viruses, including the 2019 novel coronavirus: a systematic review of ventilation and coronavirus, PLoS Glob. Public Health
Van Doremalen, Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1, N. Engl. J. Med
Vaughan, Exhaled breath condensate pH is a robust and reproducible assay of airway acidity, Eur. Respir. J
Wang, Airborne transmission of respiratory viruses, Science
Zwart, An experimental test of the independent action hypothesis in virus-insect pathosystems, Proc. Biol. Sci
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