COVID-19; SARS-CoV-2; air quality; airborne transmission; indoor; mitigation measures
Abstract :
[en] The COVID-19 pandemic due to the Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has been plaguing the world since late 2019/early 2020 and has changed the way we function as a society, halting both economic and social activities worldwide. Classrooms, offices, restaurants, public transport, and other enclosed spaces that typically gather large groups of people indoors, and are considered focal points for the spread of the virus. For society to be able to go "back to normal", it is crucial to keep these places open and functioning. An understanding of the transmission modes occurring in these contexts is essential to set up effective infection control strategies. This understanding was made using a systematic review, according to the Preferred Reporting Items for Systematic reviews and Meta-Analyses statement (PRISMA) 2020 guidelines. We analyze the different parameters influencing airborne transmission indoors, the mathematical models proposed to understand it, and discuss how we can act on these parameters. Methods to judge infection risks through the analysis of the indoor air quality are described. Various mitigation measures are listed, and their efficiency, feasibility, and acceptability are ranked by a panel of experts in the field. Thus, effective ventilation procedures controlled by CO2-monitoring, continued mask wearing, and a strategic control of room occupancy, among other measures, are put forth to enable a safe return to these essential places.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
de Crane D'Heysselaer, Simon; TERRA Research Centre, Gembloux Agro-Bio Tech, University of Liège, 5030 Gembloux, Belgium
Parisi, Gianni ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Lisson, Maxime ; Université de Liège - ULiège > GxABT : Services généraux du site > Site GxABT - Cabinet du Vice-recteur
Bruyère, Olivier ; Centre Hospitalier Universitaire de Liège - CHU > > Service de médecine de l'appareil locomoteur
Donneau, Anne-Françoise ; Université de Liège - ULiège > Département des sciences de la santé publique
Fontaine, Sébastien ; Université de Liège - ULiège > Département des sciences sociales
Gillet, Laurent ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Vaccinologie vétérinaire
Darcis, Gilles ; Centre Hospitalier Universitaire de Liège - CHU > > Service des maladies infectieuses - médecine interne
Thiry, Etienne ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI)
Ducatez, Mariette ; IHAP, Université de Toulouse, INRAE, ENVT, 31000 Toulouse, France
Snoeck, Chantal J ; Clinical and Applied Virology Group, Department of Infection and Immunity, Luxembourg Institute of Health, 4354 Esch-sur-Alzette, Luxembourg
Zientara, Stéphan ; UMR1161 Virologie, INRAE, Ecole Nationale Vétérinaire d'Alfort, Anses, Université Paris-Est, F-94700 Maisons-Alfort, France
Haddad, Nadia; UMR BIPAR 956, Anses, INRAE, Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, 94700 Maisons-Alfort, France
Humblet, Marie-France ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI)
Ludwig-Begall, Louisa ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Thiry, Damien ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Bactériologie vétérinaire et maladies bactériennes animales
Misset, Benoît ; Centre Hospitalier Universitaire de Liège - CHU > > Service des soins intensifs
Lambermont, Bernard ; Centre Hospitalier Universitaire de Liège - CHU > > Service des soins intensifs
Tandjaoui-Lambiotte, Yacine; Laboratoire Hypoxie and Poumon INSERM U1272, Service de Réanimation Médico-Chirurgicale, CHU Avicenne, Assistance Publique-Hôpitaux de Paris, 93000 Bobigny, France
Zahar, Jean-Raph; CHU Avicenne-APHP, 93000 Bobigny, France
Sartor, Kevin ; Université de Liège - ULiège > Département d'aérospatiale et mécanique > Systèmes énergétiques
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Haubruge, Eric ; Université de Liège - ULiège > GxABT : Services généraux du site > Site GxABT - Gestion de site
This systematic review was funded by the University of Liège, under a strategic opportunity credit to build an institutional Risk Management Cockpit for COVID-19.
WHO World Health Organization—Convened Global Study of Origins of SARS-CoV-2: China Part. Joint WHO-China Study (14 January–10 February 2021) 2021 Available online: https://www.who.int/publications/i/item/who-convened-global-study-of-origins-of-sars-cov-2-china-part (accessed on 16 April 2022)
WHO World Health Organization Coronavirus (COVID-19) Dashboard. WHO Coronavirus (COVID-19) Dashboard with Vaccination Data 2022 Available online: https://covid19.who.int/ (accessed on 1 October 2022)
Thanh Le T. Andreadakis Z. Kumar A. Román R.G. Tollefsen S. Saville M. Mayhew S. The COVID-19 vaccine development landscape Nat. Rev. Drug Discov. 2020 19 305 306 10.1038/d41573-020-00073-5
So A.D. Woo J. Special Paper: Reserving coronavirus disease 2019 vaccines for global access: Cross sectional analysis BMJ 2020 371 m4750 10.1136/bmj.m4750 33323376
Mathieu E. Ritchie H. Ortiz-Ospina E. Roser M. Hasell J. Appel C. Giattino C. Rodés-Guirao G. A global database of COVID-19 vaccinations Nat. Hum. Behav. 2021 5 947 953 10.1038/s41562-021-01122-8
Moriyama M. Hugentobler W.J. Iwasaki A. Seasonality of Respiratory Viral Infections Annu. Rev. Virol. 2020 7 83 101 10.1146/annurev-virology-012420-022445 32196426
Kohanski M.A. Lo L.J. Waring M.S. Review of indoor aerosol generation, transport, and control in the context of COVID-19 Int. Forum Allergy Rhinol. 2020 10 1173 1179 10.1002/alr.22661 32652898
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 10.1126/science.abd9149 34446582
Tang J.W. Bahnfleth W.P. Bluyssen P.M. Buonanno G. Jimenez J.L. Kurnitski J. Li Y. Miller S. Sekhar C. Morawska L. et al. Dismantling myths on the airborne transmission of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) J. Hosp. Infect. 2021 110 89 96 10.1016/j.jhin.2020.12.022 33453351
Chirico F. Sacco A. Bragazzi N.L. Magnavita N. Can Air-Conditioning Systems Contribute to the Spread of SARS/MERS/COVID-19 Infection? Insights from a Rapid Review of the Literature Int. J. Environ. Res. Public Health 2020 17 6052 10.3390/ijerph17176052
Da Silva P.G. Nascimento M.S.J. Soares R.R.G. Sousa S.I.V. Mesquita J.R. Airborne spread of infectious SARS-CoV-2: Moving forward using lessons from SARS-CoV and MERS-CoV Sci. Total Environ. 2021 76 e142802 10.1016/j.scitotenv.2020.142802
Burridge H.C. Fan S. Jones R.L. Noakes C.J. Linden P.F. Predictive and retrospective modelling of airborne infection risk using monitored carbon dioxide Indoor Built Environ. 2021 31 1363 1380 10.1177/1420326X211043564
Jones B. Sharpe P. Iddon C. Hathway E.A. Noakes C.J. Fitzgeralde S. Modelling uncertainty in the relative risk of exposure to the SARS-CoV-2 virus by airborne aerosol transmission in well mixed indoor air Build. Environ. 2020 191 e107617 10.1016/j.buildenv.2021.107617 33495667
Lelieveld J. Helleis F. Borrman S. Cheng Y. Drewnick F. Haug G. Klimach T. Sciare J. Su H. Pösch U. Model Calculations of Aerosol Transmission and Infection Risk of COVID-19 in Indoor Environments Int. J. Environ. Res. Public Health 2020 17 8114 10.3390/ijerph17218114 33153155
Azuma K. Yanagi U. Kagi N. Kim H. Ogata M. Hayashi M. Environmental factors involved in SARS-CoV-2 transmission: Effect and role of indoor environmental quality in the strategy for COVID-19 infection control Environ. Health Prev. Med. 2020 25 66 10.1186/s12199-020-00904-2 33143660
Bazant M.Z. Bush J.W.M. A guideline to limit indoor airborne transmission of COVID-19 Proc. Natl. Acad. Sci. USA 2021 118 e2018995118 10.1073/pnas.2018995118
Stabile L. Pacitto A. Mikszewski A. Morawska L. Buonanno G. Ventilation procedures to minimize the airborne transmission of viruses in classrooms Build. Environ. 2021 202 e108042 10.1016/j.buildenv.2021.108042
Xie W. Yanpeng Li Y. Bai W. Hou J. Ma T. Zeng X. Zhang L. An T. The source and transport of bioaerosols in the air: A review Front. Environ. Sci. Eng. 2021 15 44 10.1007/s11783-020-1336-8
Santurtún A. Colom M.L. Fdez-Arroyabe P. Del Real P. Fernández-Olmo Zarrabeitia M.T. Exposure to particulate matter: Direct and indirect role in the COVID-19 pandemic Environ. Res. 2021 206 e112261 10.1016/j.envres.2021.112261
Aganovic A. Bi Y. Cao G. Drangsholt F. Kurnitski J. Wargocki P. Estimating the impact of indoor relative humidity on SARS-CoV-2 airborne transmission risk using a new modification of the Wells-Riley model Build. Environ. 2021 205 e108278 10.1016/j.buildenv.2021.108278
Smieszek T. Lazzari G. Salathé M. Assessing the Dynamics and Control of Droplet- and Aerosol-Transmitted Influenza Using an Indoor Positioning System Sci. Rep. 2019 9 2185 10.1038/s41598-019-38825-y
Page M.J. McKenzie J.E. Bossuyt P.M. Boutron I. Hoffmann T.C. Mulrow C.D. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews Br. Med. J. 2021 372 71 10.1136/bmj.n71
Chatterjee S. Murallidharan J.S. Agrawal A. Bhardwaj R. How coronavirus survives for hours in aerosols Phys. Fluids 2021 33 081708 10.1063/5.0059908 34471334
Netz R.R. Mechanisms of Airborne Infection via Evaporating and Sedimenting Droplets Produced by Speaking J. Phys. Chem. B 2020 124 7093 7101 10.1021/acs.jpcb.0c05229 32668904
Srinivasan A. Krishan J. Bathula S. Mayya Y.S. Modeling the viral load dependence of residence times of virus-laden droplets from COVID-19-infected subjects in indoor environments Indoor Air 2021 31 1786 1797 10.1111/ina.12868
Bazant M.Z. Martin Z. Bazant M.Z. Kodio O. Cohen A.E. Khan K. Gu Z. Bush J.W.M. Monitoring carbon dioxide to quantify the risk of indoor airborne transmission of COVID-19 Flow 2021 1 E10 10.1017/flo.2021.10
Delikhoon M. Guzman M.I. Nabizadeh R. Norouzian E. Baghani A. Modes of Transmission of Severe Acute Respiratory Syndrome-Coronavirus-2 (SARS-CoV-2) and Factors Influencing on the Airborne Transmission: A Review Int. J. Environ. Res. Public Health 2021 18 395 10.3390/ijerph18020395 33419142
Pal R. Sarkar S. Mukhopadhyay A. Influence of ambient conditions on evaporation and transport of respiratory droplets in indoor environment Int. Commun. Heat Mass Transf. 2021 129 e105750 10.1016/j.icheatmasstransfer.2021.105750
Coleman K. Tay D. Tan K. Ong S. Than T. Koh M. Chin Y. Nasir H. Mak T. Chu J. et al. Viral Load of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) in Respiratory Aerosols Emitted by Patients With Coronavirus Disease 2019 (COVID-19) While Breathing, Talking, and Singing Clin. Infect. Dis. 2022 74 1722 1728 10.1093/cid/ciab691
Trancossi M. Carli C. Cannistraro G. Pascoa J. Sharma S. Could thermodynamics and heat and mass transfer research produce a fundamental step advance toward and significant reduction of SARS-COV-2 spread? Int. J. Heat Mass Transf. 2021 170 e120983 10.1016/j.ijheatmasstransfer.2021.120983
Spena A. Palombi L. Corcione M. Carestia M. Spena V.A. On the Optimal Indoor Air Conditions for SARS-CoV-2 Inactivation. An Enthalpy-Based Approach Int. J. Environ. Res. Public Health 2020 17 6083 10.3390/ijerph17176083
Riley E.C. Murphy G. Riley R.L. Airborne spread of measles in a suburban elementary school Am. J. Epidemiol. 1978 107 421 432 10.1093/oxfordjournals.aje.a112560
Shen J. Kong M. Dong B. Birnkrant M.J. Zhang J. Airborne transmission of SARS-CoV-2 in indoor environments: A comprehensive review Sci. Technol. Built Environ. 2021 27 1331 1336 10.1080/23744731.2021.1977693
Buonanno G. Stabile L. Morawska L. Estimation of airborne viral emission: Quanta emission rate of SARS-CoV-2 for infection risk assessment Environ. Int. 2020 141 e105794 10.1016/j.envint.2020.105794
Dai H. Zhao B. Association of the infection probability of COVID-19 with ventilation rates in confined spaces Build. Simul. 2020 13 1321 1327 10.1007/s12273-020-0703-5 32837691
Miller S.L. Nazaroff W.W.N. Jimenez J.L. Boerstra A. Buonanno G. Dancer S.J. Kurnitski J. Mar L.C. Morawska L. Noakes K. Transmission of SARS-CoV-2 by inhalation of respiratory aerosol in the Skagit Valley Chorale superspreading event Indoor Air 2021 31 314 323 10.1111/ina.12751 32979298
Kurnitski S.J. Martin Kiil M. Wargocki P. Boersta A. Seppänen O. Olesen B. Morawska L. Respiratory infection risk-based ventilation design method Build. Environ. 2021 206 e108387 10.1016/j.buildenv.2021.108387 34602721
Shen J. Kong M. Dong B. Birnkrant M.J. Zhang J. A systematic approach to estimating the effectiveness of multi-scale IAQ strategies for reducing the risk of airborne infection of SARS-CoV-2 Build. Environ. 2021 200 e107926 10.1016/j.buildenv.2021.107926 33967376
Beggs C.B. Avital E.J. A psychrometric model to assess the biological decay of the SARS-CoV-2 virus in aerosols Peer J. 2021 9 e11024 10.7717/peerj.11024 33717712
Quraishi S.A. Berra L. Nozari A. Indoor temperature and relative humidity in hospitals: Workplace considerations during the novel coronavirus pandemic Occup. Environ. Med. 2020 77 508 10.1136/oemed-2020-106653
Biryukov J. Boydston J.A. Dunning R.A. Yeager J.J. Wood S. Reese A.L. Ferris A. Miller D. Weaver W. Zeitouni N.E. et al. Increasing Temperature and Relative Humidity Accelerates Inactivation of SARS-CoV-2 on Surfaces mSphere 2020 5 e00441-20 10.1128/mSphere.00441-20
Elsaid A.M. Mohamed H.A. Abdelaziz G.B. Ahmed M.S. A critical review of heating, ventilation, and air conditioning (HVAC) systems within the context of a global SARS-CoV-2 epidemic Process Saf. Environ. Prot. 2021 155 230 261 10.1016/j.psep.2021.09.021
Bu Y. Ooka R. Kikumoto H. Oh W. Recent research on expiratory particles in respiratory viral infection and control strategies: A review Sustain. Cities Soc. 2021 73 e103106 10.1016/j.scs.2021.103106
Vassella C.C. Koch J. Henzi A. Jordan A. Waeber R. Iannaccone R. Charrière R. From spontaneous to strategic natural window ventilation: Improving indoor air quality in Swiss schools Int. J. Hyg. Environ. Health 2021 234 e113746 10.1016/j.ijheh.2021.113746
Peng Z. Jimenez J.L. Exhaled CO2 as a COVID-19 infection risk proxy for different indoor environments and activities Environ. Sci. Technol. Lett. 2021 8 392 397 10.1021/acs.estlett.1c00183
Vouriot C.V.M. Burridge H.C. Noakes C.J. Linden P.F. Seasonal variation in airborne infection risk in schools due to changes in ventilation inferred from monitored carbon dioxide Indoor Air 2021 31 1154 1163 10.1111/ina.12818 33682974
Chillon S.A. Millan M. Aramendia I. Unai Fernandez-Gamiz U. Zulueta E. Mendaza-Sagastizabal X. Natural Ventilation Characterization in a Classroom under Different Scenarios Int. J. Environ. Res. Public Health 2021 18 5425 10.3390/ijerph18105425 34069502
Lepore E. Aguilera Benito P. Piña Ramírez C. Viccione G. Indoors ventilation in times of confinement by SARS-CoV-2 epidemic: A comparative approach between Spain and Italy Sustain. Cities Soc. 2021 72 e103051 10.1016/j.scs.2021.103051
Morawska L. Tang J.W. Bahnfleth W. Bluyssen P.M. Boerstra A. Buonanno G. Cao J. Dancer S. Floto A. Franchimon F. et al. How can airborne transmission of COVID-19 indoors be minimised? Environ. Int. 2020 142 e105832 10.1016/j.envint.2020.105832
Lung D.C. Kwan M.Y.W. Chow C.B. Airborne transmission of SARS-CoV-2: Ventilation improvement strategies in preparation for school re-opening Hong Kong Med. J. 2021 27 328 329 10.12809/hkmj215122
Lee H. Ahn K.-H. Estimate of the critical exposure time based on 70 confirmed COVID-19 cases J. Korean Phys. Soc. 2021 79 492 498 10.1007/s40042-021-00225-9
Aguilar A.J. De La Hoz-Torres M.L. Martínez-Aires M.D. Ruiz D.P. Monitoring and Assessment of Indoor Environmental Conditions after the Implementation of COVID-19-Based Ventilation Strategies in an Educational Building in Southern Spain Sensors 2021 21 7223 10.3390/s21217223
Rodríguez M. Palop M.L. Seseña S. Rodríguez A. Are the Portable Air Cleaners (PAC) really effective to terminate airborne SARS-CoV-2? Sci. Total Environ. 2021 785 e147300 10.1016/j.scitotenv.2021.147300 33940414
Bono N. Ponti F. Punta C. Candiani G. Effect of UV irradiation and TiO2-photocatalysis on airborne bacteria and viruses: An overview Materials 2021 14 1075 10.3390/ma14051075 33669103
García de Abajo F.J. Javier Hernández R. Kaminer I. Meyerhans A. Rosell-Llompart J. Sanchez-Elsner T. Back to Normal: An Old Physics Route to Reduce SARS-CoV-2 Transmission in Indoor Spaces ACS Nano 2020 14 7704 7713 10.1021/acsnano.0c04596 32551537
Standard 62.1-2019 Ventilation for Acceptable Indoor Air Quality ASHRAE Atlanta, GA, USA 2019 87p
Melikov A.K. Ai Z.T. Markov D.G. Intermittent occupancy combined with ventilation: An efficient strategy for the reduction of airborne transmission indoors Sci. Total Environ. 2020 744 e140908 10.1016/j.scitotenv.2020.140908
Park S. Choi Y. Song D. Kim E.K. Natural ventilation strategy and related issues to prevent coronavirus disease 2019 (COVID-19) airborne transmission in a school building Sci. Total Environ. 2021 789 e147764 10.1016/j.scitotenv.2021.147764
Rencken G.K. Rutherford E.K. Ghanta N. Kongoletos J. Glicksman L. Patterns of SARS-CoV-2 aerosol spread in typical classrooms Build. Environ. 2021 204 e108167 10.1016/j.buildenv.2021.108167
Singer B.C. Zhao H. Preble C.V. Delp W.W. Pantelic J. Sohn M.D. Kirchstetter T.W. Measured influence of overhead on exposure to airborne contaminants from simulated speaking in a meeting and a classroom Indoor Air 2022 32 e12917 10.1111/ina.12917
Ascione F. De Masi R.F. Mastellone M. Vanoli G.P. The design of safe classrooms of educational buildings for facing contagions and transmission of diseases: A novel approach combining audits, calibrated energy models, building performance (BPS) and computational fluid dynamic (CFD) simulations Energy Build. 2021 230 e110533 10.1016/j.enbuild.2020.110533
Duill F.F. Florian Schulz F. Jain A. Krieger L. van Wachem B. Beyrau F. The Impact of Large Mobile Air Purifiers on Aerosol Concentration in Classrooms and the Reduction of Airborne Transmission of SARS-CoV-2 Int. J. Environ. Res. Public Health 2021 18 11523 10.3390/ijerph182111523
Gil-Baez M. Lizana J. Becerra Villanueva J.A. Molina-Huelva M. Serrano-Jimenez A. Chacartegui R. Natural ventilation in classrooms for healthy schools in the COVID era in Mediterranean climate Build. Environ. 2021 206 e108345 10.1016/j.buildenv.2021.108345
Kulo A. Klarić S. Ćetković A. Blekić A. Kusturica A. Spahić N. Armin Šljivo A. Šečić D. School children exposure to low indoor air quality in classrooms during covid-19 pandemic: Results of a pilot study Psychiatr. Danub. 2021 33 83 94 10.5005/sar-1-1-2-83
Nazarenko Y. Air filtration and SARS-CoV-2 Epidemiol. Health 2020 42 e2020049 10.4178/epih.e2020049 32660218
De Almeida D.S. Droprinchinski Martins L. Curti Muniz E. Rudke A.P. Squizzato R. Beal F.A. de Souza P.R. Patrícia D. Bonfim F. Lopes Aguiar M. et al. Biodegradable CA/CPB electrospun nanofibers for efficient retention of airborne nanoparticles Process Saf. Environ. Prot. 2020 144 177 185 10.1016/j.psep.2020.07.024 32834561
De Almeida D.S. Scacchetti F.A.P. Santos R. Lopes Aguiar M. Beal A. Anderson P. Rudke A.P. de Souza Santana M.H. Valério Lisboa A.M. Bezerra F.M. et al. Evaluation of biocidal properties of biodegradable nanofiber filters and their use in face masks Environ. Technol. 2021 9 e1982020 10.1080/09593330.2021.1982020 34524952
Lendvay T.S. Chen J. Harcourt B.H. Scholte F.E.M. Lin Y.L. Kilinc-Balci F.S. Lamb M.M. Homdayjanakul K. Cui Y. Price A. et al. Addressing personal protective equipment (PPE) decontamination: Methylene blue and light inactivates SARS-COV-2 on N95 respirators and medical masks with maintenance of integrity and fit Infect. Control. Hosp. Epidemiol. 2022 43 876 885 10.1017/ice.2021.230 34016200
Kwon T.K. Gaudreault N.N. Richt J.A. Seasonal stability of SARS-CoV-2 in biological fluids Pathogens 2021 10 540 10.3390/pathogens10050540 33946190