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

S Jaumdally; M Tomasicchio; A Pooran; A Esmail; A Kotze; S Meier; L Wilson; S Oelofse; C van der Merwe; A Roomaney; M Davids; T Suliman; R Joseph; T Perumal; A Scott; M Shaw; W Preiser; C Williamson; A Goga; E Mayne; G Gray; P Moore; A Sigal; J Limberis; J Metcalfe; K Dheda

doi:10.1038/s41467-024-45400-1

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

Nat Commun. 2024 Mar 5;15(1):2003. doi: 10.1038/s41467-024-45400-1.

Authors

S Jaumdally^{1

2}, M Tomasicchio^{1

2}, A Pooran^{1

2}, A Esmail^{1

2}, A Kotze^{1

2}, S Meier^{1

2}, L Wilson^{1

2}, S Oelofse^{1

2}, C van der Merwe^{1

2}, A Roomaney^{1

2}, M Davids^{1

2}, T Suliman³, R Joseph⁴, T Perumal^{1

2}, A Scott^{1

2}, M Shaw³, W Preiser⁵, C Williamson^{4

6

7}, A Goga^{8

9}, E Mayne^{10

11

12}, G Gray¹³, P Moore^{6

14

15}, A Sigal^{16

17

18}, J Limberis¹⁹, J Metcalfe¹⁹, K Dheda^{20

21

22}

Affiliations

¹ Division of Pulmonology, Department of Medicine, Centre for Lung Infection and Immunity, University of Cape Town Lung Institute, Cape Town, South Africa.
² Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa.
³ Department of Medical Biosciences, University of the Western Cape, Cape Town, South Africa.
⁴ 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.
⁵ 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.
⁶ Centre for the AIDS Programme of Research in South Africa (CAPRISA), Durban, South Africa.
⁷ National Health Laboratory Service (NHLS), Cape Town, South Africa.
⁸ HIV and Other Infectious Diseases Research Unit, South African Medical Research Council, Pretoria, South Africa.
⁹ Department of Paediatrics and Child Health, University of Pretoria, Pretoria, South Africa.
¹⁰ Department of Immunology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
¹¹ National Health Laboratory Services, Johannesburg, South Africa.
¹² Division of Immunology, Department of Pathology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa.
¹³ South African Medical Research Council, Cape Town, South Africa.
¹⁴ National Institute for Communicable Diseases of the National Health Laboratory Service, Johannesburg, South Africa.
¹⁵ SA MRC Antibody Immunity Research Unit, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
¹⁶ Africa Health Research Institute, Durban, South Africa.
¹⁷ School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.
¹⁸ Max Planck Institute for Infection Biology, Berlin, Germany.
¹⁹ Division of Pulmonary and Critical Care Medicine, Zuckerberg San Francisco General Hospital and Trauma Centre, University of California, San Francisco, San Francisco, CA, USA.
²⁰ 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.
²¹ Centre for the Study of Antimicrobial Resistance, South African Medical Research Council, Cape Town, South Africa. keertan.dheda@uct.ac.za.
²² Department of Infection Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK. keertan.dheda@uct.ac.za.

Abstract

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.

MeSH terms

COVID-19*
Humans
Kinetics
Respiratory Aerosols and Droplets
SARS-CoV-2*

Supplementary concepts

SARS-CoV-2 variants

Grants and funding

WT_/Wellcome Trust/United Kingdom