Frequency, kinetics and determinants of viable SARS-CoV-2 in bioaerosols from ambulatory COVID-19 patients infected with the Beta, Delta or Omicron variants.

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
05 Mar 2024
Historique:
received: 04 10 2023
accepted: 22 01 2024
medline: 6 3 2024
pubmed: 6 3 2024
entrez: 5 3 2024
Statut: epublish

Résumé

Airborne transmission of SARS-CoV-2 aerosol remains contentious. Importantly, whether cough or breath-generated bioaerosols can harbor viable and replicating virus remains largely unclarified. We performed size-fractionated aerosol sampling (Andersen cascade impactor) and evaluated viral culturability in human cell lines (infectiousness), viral genetics, and host immunity in ambulatory participants with COVID-19. Sixty-one percent (27/44) and 50% (22/44) of participants emitted variant-specific culture-positive aerosols <10μm and <5μm, respectively, for up to 9 days after symptom onset. Aerosol culturability is significantly associated with lower neutralizing antibody titers, and suppression of transcriptomic pathways related to innate immunity and the humoral response. A nasopharyngeal Ct <17 rules-in ~40% of aerosol culture-positives and identifies those who are probably highly infectious. A parsimonious three transcript blood-based biosignature is highly predictive of infectious aerosol generation (PPV > 95%). There is considerable heterogeneity in potential infectiousness i.e., only 29% of participants were probably highly infectious (produced culture-positive aerosols <5μm at ~6 days after symptom onset). These data, which comprehensively confirm variant-specific culturable SARS-CoV-2 in aerosol, inform the targeting of transmission-related interventions and public health containment strategies emphasizing improved ventilation.

Identifiants

DOI: 10.1038/s41467-024-45400-1 PMID: 38443359
pubmed: 38443359
doi: 10.1038/s41467-024-45400-1
pii: 10.1038/s41467-024-45400-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2003

Subventions

Organisme : South African Medical Research Council (SAMRC)
ID : MRC - 501Y, V2 - CASS

Informations de copyright

© 2024. The Author(s).

Références

WHO Coronavirus (COVID-19) Dashboard https://covid19.who.int/ (World Health Organization, 2023).
Fennelly, K. P. Particle sizes of infectious aerosols: implications for infection control. Lancet Respir. Med. 8, 914–924 (2020).
doi: 10.1016/S2213-2600(20)30323-4 pubmed: 32717211 pmcid: 7380927
Guerin, L. F. & Mitchell, C. A. A method for determining the concentration of air borne virus and sizing droplet nuclei containing the agent. Can. J. Comp. Med. Vet. Sci. 28, 283–287 (1964).
pubmed: 17649542 pmcid: 1494346
Fennelly, K. et al. Collection and measurement of aerosols of viable influenza virus in liquid media in an Andersen cascade impactor. Virus Adapt. Treat. 7, 1–9 (2015).
Theron, G. et al. Bacterial and host determinants of cough aerosol culture positivity in patients with drug-resistant versus drug-susceptible tuberculosis. Nat. Med. 26, 1435–1443 (2020).
doi: 10.1038/s41591-020-0940-2 pubmed: 32601338 pmcid: 8353872
Williams, C. M. et al. Exhaled SARS-CoV-2 quantified by face-mask sampling in hospitalised patients with COVID-19. J. Infect. 82, 253–259 (2021).
doi: 10.1016/j.jinf.2021.03.018 pubmed: 33774019 pmcid: 7989096
Lednicky, J. A. et al. Viable SARS-CoV-2 in the air of a hospital room with COVID-19 patients. Int. J. Infect. Dis. 100, 476–482 (2020).
doi: 10.1016/j.ijid.2020.09.025 pubmed: 32949774 pmcid: 7493737
William, B. V. et al. Viable SARS-CoV-2 Delta variant detected in aerosols in a residential setting with a self-isolating college student with COVID-19. J. Aerosol. Sci. 165, 106038 (2022).
doi: 10.1016/j.jaerosci.2022.106038
Silva, P. G., Branco, P. T. B. S., Soares, R. R. G., Mesquita, J. R. & Sousa, S. I. V. SARS-CoV-2 air sampling: a systematic review on the methodologies for detection and infectivity. Indoor Air. 32, e13083 (2022).
doi: 10.1111/ina.13083 pubmed: 36040285 pmcid: 9538005
Greenhalgh, T. et al. Ten scientific reasons in support of airborne transmission of SARS-CoV-2. Lancet 397, 1603–1605 (2021).
doi: 10.1016/S0140-6736(21)00869-2 pubmed: 33865497 pmcid: 8049599
Eichler, N. et al. Transmission of severe acute respiratory syndrome coronavirus 2 during border quarantine and air travel, New Zealand (Aotearoa). Emerg. Infect. Dis. 27, 1274–1278 (2021).
doi: 10.3201/eid2705.210514 pubmed: 33734063 pmcid: 8084504
Tang, S. et al. Aerosol transmission of SARS-CoV-2? Evidence, prevention and control. Environ. Int. 144, 106039 (2020).
doi: 10.1016/j.envint.2020.106039 pubmed: 32822927 pmcid: 7413047
Klompas, M. et al. A SARS-CoV-2 cluster in an acute care hospital. Ann. Intern. Med. 174, 794–802 (2021).
doi: 10.7326/M20-7567 pubmed: 33556277
Kutter, J. S. et al. SARS-CoV and SARS-CoV-2 are transmitted through the air between ferrets over more than one meter distance. Nat. Commun. 12, 1653 (2021).
doi: 10.1038/s41467-021-21918-6 pubmed: 33712573 pmcid: 7955093
Sia, S. F. et al. Pathogenicity, transmissibility, and fitness of SARS-CoV-2 Omicron in Syrian hamsters. Science 377, 428–433 (2022).
doi: 10.1126/science.abn8939
Santarpia, J. L. et al. The size and culturability of patient-generated SARS-CoV-2 aerosol. J. Expo. Sci. Environ. Epidemiol. 32, 706–711 (2021).
doi: 10.1038/s41370-021-00376-8 pubmed: 34408261 pmcid: 8372686
Adenaiye, O. O. et al. Infectious severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in exhaled aerosols and efficacy of masks during early mild infection. Clin. Infect. Dis. 75, e241–e248 (2022).
doi: 10.1093/cid/ciab797 pubmed: 34519774
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359 (2005).
doi: 10.1038/nature04153 pubmed: 16292310 pmcid: 7094981
Puhach, O., Meyer, B. & Eckerle, I. SARS-CoV-2 viral load and shedding kinetics. Nat. Rev. Microbiol. 22, 1–15 (2022).
Johnson, T. J. et al. Viral load of SARS-CoV-2 in droplets and bioaerosols directly captured during breathing, speaking and coughing. Sci. Rep. 12, 3484 (2022).
doi: 10.1038/s41598-022-07301-5 pubmed: 35241703 pmcid: 8894466
Ong, S. W. X. et al. Lack of viable severe acute respiratory coronavirus virus 2 (SARS-CoV-2) among PCR-positive air samples from hospital rooms and community isolation facilities. Infect. Control Hosp. Epidemiol. 42, 1327–1332 (2021).
doi: 10.1017/ice.2021.8 pubmed: 33487210
Heneghan, C. et al. SARS-CoV-2 and the role of airborne transmission: a systematic review. F1000 Res. 10, 232 (2021).
doi: 10.12688/f1000research.52091.2
Kawahara, T. et al. Characteristics of SARS-CoV-2 super-spreaders in Japan. J. Infect. 84, e6–e9 (2022).
doi: 10.1016/j.jinf.2021.12.036 pubmed: 34974057
Adam, D. C. et al. Clustering and superspreading potential of SARS-CoV-2 infections in Hong Kong. Nat. Med. 26, 1714–1719 (2020).
doi: 10.1038/s41591-020-1092-0 pubmed: 32943787
Johansson, M. A. et al. SARS-CoV-2 transmission from people without COVID-19 symptoms. JAMA Netw. Open. 4, e2035057 (2021).
doi: 10.1001/jamanetworkopen.2020.35057 pubmed: 33410879 pmcid: 7791354
Hakki, S. et al. Onset and window of SARS-CoV-2 infectiousness and temporal correlation with symptom onset: a prospective, longitudinal, community cohort study. Lancet Respir. Med. 10, 1061–1073 (2022).
doi: 10.1016/S2213-2600(22)00226-0 pubmed: 35988572 pmcid: 9388060
Scully, R. P. COVID vaccines slash risk of spreading Omicron — and so does previous infection. Nature. https://www.nature.com/articles/d41586-022-02328-0 (26 August 2022).
Vastrad, B., Vastrad, C. & Tengli, A. Bioinformatics analyses of significant genes, related pathways, and candidate diagnostic biomarkers and molecular targets in SARS-CoV-2/COVID-19. Gene Rep. 21, 100956 (2020).
doi: 10.1016/j.genrep.2020.100956 pubmed: 33553808 pmcid: 7854084
Afzali, B., Noris, M., Lambrecht, B. N. & Kemper, C. The state of complement in COVID-19. Nat. Rev. Immunol. 22, 77–84 (2022).
doi: 10.1038/s41577-021-00665-1 pubmed: 34912108
Stein, S. R. et al. SARS-CoV-2 infection and persistence in the human body and brain at autopsy. Nature 612, 758–763 (2022).
doi: 10.1038/s41586-022-05542-y pubmed: 36517603 pmcid: 9749650
Chavan, S. S., Pavlov, V. A. & Tracey, K. J. Mechanisms and therapeutic relevance of neuro-immune communication. Immunity 46, 927–942 (2017).
doi: 10.1016/j.immuni.2017.06.008 pubmed: 28636960 pmcid: 5578398
Kistemaker, L. E. M. & Gosens, R. Acetylcholine beyond bronchoconstriction: roles in inflammation and remodeling. Trends Pharm. Sci. 36, 164–171 (2015).
doi: 10.1016/j.tips.2014.11.005 pubmed: 25511176
Mistry, P. et al. SARS-CoV-2 variants, vaccines, and host immunity. Front. Immunol. 12, 809244 (2022).
doi: 10.3389/fimmu.2021.809244 pubmed: 35046961 pmcid: 8761766
Song, W. J. et al. Confronting COVID-19-associated cough and the post-COVID syndrome: role of viral neurotropism, neuroinflammation, and neuroimmune responses. Lancet Respir. Med. 9, 533–544 (2021).
doi: 10.1016/S2213-2600(21)00125-9 pubmed: 33857435 pmcid: 8041436
Lu, X. et al. US CDC real-time reverse transcription PCR panel for detection of severe acute respiratory syndrome coronavirus 2. Emerg. Infect. Dis. 26, 1654–1665 (2020).
doi: 10.3201/eid2608.201246 pubmed: 32396505 pmcid: 7392423
Tzou, P. L., Tao, K., Pond, S. L. K. & Shafer, R. W. Coronavirus resistance database (CoV-RDB): SARS-CoV-2 susceptibility to monoclonal antibodies, convalescent plasma, and plasma from vaccinated persons. PloS One 17, e0261045 (2022).
doi: 10.1371/journal.pone.0261045 pmcid: 8906623

Auteurs

S Jaumdally (S)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

M Tomasicchio (M)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

A Pooran (A)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

A Esmail (A)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

A Kotze (A)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

S Meier (S)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

L Wilson (L)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

S Oelofse (S)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

C van der Merwe (C)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

A Roomaney (A)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

M Davids (M)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.

T Suliman (T)

Department of Medical Biosciences, University of the Western Cape, Cape Town, South Africa.

R Joseph (R)

Division of Medical Virology, Wellcome Centre for Infectious Diseases in Africa, Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa.

T Perumal (T)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.
ORCID: 0000-0003-0679-5804

A Scott (A)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.
ORCID: 0000-0003-0647-607X

M Shaw (M)

Department of Medical Biosciences, University of the Western Cape, Cape Town, South Africa.
ORCID: 0000-0002-1267-0891

W Preiser (W)

Division of Medical Virology, Faculty of Medicine and Health Sciences, University of Stellenbosch Tygerberg Campus; Medical Virology, National Health Laboratory Service Tygerberg, Parow, Cape Town, South Africa.
ORCID: 0000-0002-0254-7910

C Williamson (C)

Division of Medical Virology, Wellcome Centre for Infectious Diseases in Africa, Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa.
Centre for the AIDS Programme of Research in South Africa (CAPRISA), Durban, South Africa.
National Health Laboratory Service (NHLS), Cape Town, South Africa.
ORCID: 0000-0003-0125-1226

A Goga (A)

HIV and Other Infectious Diseases Research Unit, South African Medical Research Council, Pretoria, South Africa.
Department of Paediatrics and Child Health, University of Pretoria, Pretoria, South Africa.

E Mayne (E)

Department of Immunology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
National Health Laboratory Services, Johannesburg, South Africa.
Division of Immunology, Department of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa.
ORCID: 0000-0002-6360-3488

G Gray (G)

South African Medical Research Council, Cape Town, South Africa.

P Moore (P)

Centre for the AIDS Programme of Research in South Africa (CAPRISA), Durban, South Africa.
National Institute for Communicable Diseases of the National Health Laboratory Service, Johannesburg, South Africa.
SA MRC Antibody Immunity Research Unit, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
ORCID: 0000-0001-8719-4028

A Sigal (A)

Africa Health Research Institute, Durban, South Africa.
School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.
Max Planck Institute for Infection Biology, Berlin, Germany.
ORCID: 0000-0001-8571-2004

J Limberis (J)

Division of Pulmonary and Critical Care Medicine, Zuckerberg San Francisco General Hospital and Trauma Centre, University of California, San Francisco, San Francisco, CA, USA.
ORCID: 0000-0002-7893-8416

J Metcalfe (J)

Division of Pulmonary and Critical Care Medicine, Zuckerberg San Francisco General Hospital and Trauma Centre, University of California, San Francisco, San Francisco, CA, USA.

K Dheda (K)

Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa. keertan.dheda@uct.ac.za.
Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa. keertan.dheda@uct.ac.za.
Department of Infection Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK. keertan.dheda@uct.ac.za.
ORCID: 0000-0001-7709-5341

Classifications MeSH