Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks

COVID-19 Genomics Belgium Consortium; Jean-Michel Dogné; Pascale Hilbert; Jonathan Degosserie; Olivier Denis

doi:10.1038/s43587-023-00421-1

Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks

COVID-19 Genomics Belgium Consortium
, Jean-Michel Dogné
, Pascale Hilbert
, Jonathan Degosserie
, Olivier Denis

Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

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Résumé

Coronavirus Disease 2019 (COVID-19) vaccination has resulted in excellent protection against fatal disease, including in older adults. However, risk factors for post-vaccination fatal COVID-19 are largely unknown. We comprehensively studied three large nursing home outbreaks (20–35% fatal cases among residents) by combining severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) aerosol monitoring, whole-genome phylogenetic analysis and immunovirological profiling of nasal mucosa by digital nCounter transcriptomics. Phylogenetic investigations indicated that each outbreak stemmed from a single introduction event, although with different variants (Delta, Gamma and Mu). SARS-CoV-2 was detected in aerosol samples up to 52 d after the initial infection. Combining demographic, immune and viral parameters, the best predictive models for mortality comprised IFNB1 or age, viral ORF7a and ACE2 receptor transcripts. Comparison with published pre-vaccine fatal COVID-19 transcriptomic and genomic signatures uncovered a unique IRF3 low/IRF7 high immune signature in post-vaccine fatal COVID-19 outbreaks. A multi-layered strategy, including environmental sampling, immunomonitoring and early antiviral therapy, should be considered to prevent post-vaccination COVID-19 mortality in nursing homes.

langue originale	Anglais
Pages (de - à)	722-733
Nombre de pages	12
journal	Nature Aging
Volume	3
Numéro de publication	6
Les DOIs	https://doi.org/10.1038/s43587-023-00421-1
Etat de la publication	Publié - juin 2023

Financement

We would like to acknowledge the numerous diagnostics laboratories involved in performing the consecutive screenings in the three nursing homes and for sharing detailed RT\u2013qPCR results. Special thanks go to the representatives of the three nursing homes for providing additional and detailed information to make this collaboration fruitful: the (nursing) staff of Nos Tayons in Nivelles (with specific support of P. Gilbert), of Les Cytises nursing home in Braives and of Ter Burg in Zaventem (with special thanks to N. Deblaere, R. Verschueren and K. Boydens). UZ Leuven, as national reference center for respiratory pathogens, is supported by Sciensano, which is gratefully acknowledged. J.M.C. was supported by the HONOURs Marie-Sklodowska-Curie training network (grant 721367). This work is also supported by \u2018Interne Fondsen KU Leuven/Internal Funds KU Leuven\u2019 project 3M170314 and C3/20/105 awarded to P.M. The sequencing capacity of this work was supported, in part, by a COVID-19 research grant of \u2018Fonds Wetenschappelijk Onderzoek\u2019/Research Foundation Flanders (grant G0H4420N) awarded to P.M., G.B. and E.A. S.D. is supported by the \u2018Fonds National de la Recherche Scientifique\u2019 (FNRS, Belgium) and by the European Union Horizon 2020 project MOOD (grant agreement no. 874850). G.B. acknowledges support from the Internal Funds KU Leuven (grant C14/18/094) and from the Research Foundation\u2013Flanders (\u2018Fonds voor Wetenschappelijk Onderzoek\u2013Vlaanderen\u2019, G0E1420N and G098321N), the latter grant also for S.D. J.V.W. is supported by the Research Foundation\u2013Flanders (G0A0621N and G065421N). P.V. is a senior clinical investigator of the Research Foundation\u2013Flanders. K.K.A. is supported by Research Foundation\u2013Flanders (FWO G0G4220N). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Bailleurs de fonds	Numéro du bailleur de fonds
Fonds De La Recherche Scientifique - FNRS
Horizon 2020
KU Leuven	C14/18/094
Fonds voor Wetenschappelijk Onderzoek—Vlaanderen	G065421N, G0E1420N, G0A0621N, G098321N
Fonds Wetenschappelijk Onderzoek - Vlaanderen (FWO)	G0G4220N
HONOURs Marie-Sklodowska-Curie training network	3M170314, C3/20/105, 721367
Horizon 2020 Framework Programme	874850
Fonds Wetenschappelijk Onderzoek’/Research Foundation Flanders	G0H4420N

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title = "Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks",

abstract = "Coronavirus Disease 2019 (COVID-19) vaccination has resulted in excellent protection against fatal disease, including in older adults. However, risk factors for post-vaccination fatal COVID-19 are largely unknown. We comprehensively studied three large nursing home outbreaks (20–35\% fatal cases among residents) by combining severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) aerosol monitoring, whole-genome phylogenetic analysis and immunovirological profiling of nasal mucosa by digital nCounter transcriptomics. Phylogenetic investigations indicated that each outbreak stemmed from a single introduction event, although with different variants (Delta, Gamma and Mu). SARS-CoV-2 was detected in aerosol samples up to 52 d after the initial infection. Combining demographic, immune and viral parameters, the best predictive models for mortality comprised IFNB1 or age, viral ORF7a and ACE2 receptor transcripts. Comparison with published pre-vaccine fatal COVID-19 transcriptomic and genomic signatures uncovered a unique IRF3 low/IRF7 high immune signature in post-vaccine fatal COVID-19 outbreaks. A multi-layered strategy, including environmental sampling, immunomonitoring and early antiviral therapy, should be considered to prevent post-vaccination COVID-19 mortality in nursing homes.",

author = "\{COVID-19 Genomics Belgium Consortium\} and Lize Cuypers and Els Keyaerts and Hong, \{Samuel Leandro\} and Sarah Gorissen and Menezes, \{Soraya Maria\} and Marick Starick and \{Van Elslande\}, Jan and Matthias Weemaes and Tony Wawina-Bokalanga and Joan Marti-Carreras and Bert Vanmechelen and \{Van Holm\}, Bram and Mandy Bloemen and Jean-Michel Dogn{\'e} and Fran{\c c}ois Dufrasne and Keith Durkin and Jean Ruelle and \{De Mendonca\}, Ricardo and Elke Wollants and Pieter Vermeersch and Ruddy Wattiez and Michael Peeters and Kate Bakelants and Sarah Denayer and Dufrasne, \{Fran{\c c}ois E.\} and C{\'e}cile Meex and Laurent Gillet and Maria Artesi and Hayette, \{Marie Pierre\} and S{\'e}bastien Bontems and Vincent Bours and Claire Gourzon{\`e}s and Olivier Ek and Fabrice Bureau and Benoit Kabamba and Gala, \{Jean Luc\} and Bertrand Bearzatto and J{\'e}r{\^o}me Ambroise and Arnaud Marchant and Coralie Henin and Benoit Haerlingen and \{de Mendonca\}, Ricardo and Delforge, \{Marie Luce\} and Carl Vael and Lynsey Berckmans and Philippe Selhorst and Ari{\"e}n, \{Kevin K.\} and Pascale Hilbert and Jonathan Degosserie and Olivier Denis",

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year = "2023",

month = jun,

doi = "10.1038/s43587-023-00421-1",

language = "English",

volume = "3",

pages = "722--733",

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Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks. / COVID-19 Genomics Belgium Consortium ; Dogné, Jean-Michel ; Hilbert, Pascale et al.
Dans: Nature Aging, Vol 3, Numéro 6, 06.2023, p. 722-733.

Résultats de recherche: Contribution à un journal/une revue › Article › Revue par des pairs

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Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks

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