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

Lize Cuypers; Els Keyaerts; Samuel Leandro Hong; Sarah Gorissen; Soraya Maria Menezes; Marick Starick; Jan Van Elslande; Matthias Weemaes; Tony Wawina-Bokalanga; Joan Marti-Carreras; Bert Vanmechelen; Bram Van Holm; Mandy Bloemen; Jean Michel Dogne; François E. Dufrasne; Keith Durkin; Jean Ruelle; Ricardo de Mendonca; Elke Wollants; Pieter Vermeersch; Caroline Boulouffe; Achille Djiena; Caroline Broucke; Boudewijn Catry; Katrien Lagrou; Marc Van Ranst; Johan Neyts; Guy Baele; Piet Maes; Emmanuel André; Simon Dellicour; Johan Van Weyenbergh; COVID-19 Genomics Belgium Consortium

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

Lize Cuypers
, Els Keyaerts
, Samuel Leandro Hong
, Sarah Gorissen
, Soraya Maria Menezes
, Marick Starick
, Jan Van Elslande
, Matthias Weemaes
, Tony Wawina-Bokalanga
, Joan Marti-Carreras
, Bert Vanmechelen
, Bram Van Holm
, Mandy Bloemen
, Jean Michel Dogne
, François E. Dufrasne
, Keith Durkin
, Jean Ruelle
, Ricardo de Mendonca
, Elke Wollants
, Pieter Vermeersch

Caroline Boulouffe, Achille Djiena, Caroline Broucke, Boudewijn Catry, Katrien Lagrou, Marc Van Ranst, Johan Neyts, Guy Baele, Piet Maes, Emmanuel André, Simon Dellicour, Johan Van Weyenbergh, COVID-19 Genomics Belgium Consortium

Research output: Contribution to journal › Article › Research › peer-review

8 Citations (Scopus)

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.

Original language	English
Pages (from-to)	722-733
Number of pages	12
Journal	Nature Aging
Volume	3
Issue number	6
DOIs	https://doi.org/10.1038/s43587-023-00421-1
Publication status	Published - Jun 2023
Externally published	Yes

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

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10.1038/s43587-023-00421-1Licence: CC BY

Cite this

Cuypers, L., Keyaerts, E., Hong, S. L., Gorissen, S., Menezes, S. M., Starick, M., Van Elslande, J., Weemaes, M., Wawina-Bokalanga, T., Marti-Carreras, J., Vanmechelen, B., Van Holm, B., Bloemen, M., Dogne, J. M., Dufrasne, F. E., Durkin, K., Ruelle, J., de Mendonca, R., Wollants, E., ... COVID-19 Genomics Belgium Consortium (2023). Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks. Nature Aging, 3(6), 722-733. https://doi.org/10.1038/s43587-023-00421-1

@article{807e0b865d0540e6b145a76384b6b0c2,

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 = "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 Dogne, \{Jean Michel\} and Dufrasne, \{Fran{\c c}ois E.\} 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 \{Van Dooren\}, Sonia and Bruno Hinckel and Hideo Imamura and Toon Janssen and Ben Caljon and Oriane Soetens and Denis Pi{\'e}rard and Thomas Demuyser and Charlotte Michel and Olivier Vandenberg and \{van den Wijngaert\}, Sigi and Giulia Zorzi and \{Van Lint\}, Philippe and Walter Verstrepen and Reinout Naesens and \{Van Lent\}, Sarah and Pascale Hilbert and Sylvain Broh{\'e}e and L{\'e}onard, \{Pierre Emmanuel\} and Deniz Karadurmus and Jeremie Gras and Damien F{\'e}ret and Barbara Lambert and Anne Vankeerberghen and Astrid Holderbeke and \{De Beenhouwer\}, Hans and Lien Cattoir and Christine Lammens and Xavier, \{Basil Britto\} and \{Le Mercier\}, Marie and Jasmine Coppens and Veerle Matheeussen and Herman Goossens and Martens, \{Geert A.\} and Koen Swaerts and \{Van Hoecke\}, Frederik and Dieter Desmet and Patrick Descheemaeker and Pierre Bogaerts and Jonathan Degosserie and Olivier Denis and Huang, \{Te Din\} and Dagmar Obbels and Hanne Valgaeren and Johan Frans and Annick Smismans and Claus, \{Paul Emile\} and Denise Veltman and Truus Goegebuer and Ann Lemmens and \{Van den Poel\}, Bea and \{De Bock\}, Sonja and Wim Laffut and \{Van Even\}, Ellen and \{Van Acker\}, Jos and Charlotte Verfaillie and Elke Vanlaere and \{De Rauw\}, Klara and Luc Waumans and \{Van Meensel\}, Britt and Reinoud Cartuyvels and Marijke Raymaekers and Bruno Verhasselt and Jorn Hellemans and Merijn Vanhee and Marijke Reynders and Caroline Boulouffe and Achille Djiena and Caroline Broucke and Boudewijn Catry and Katrien Lagrou and \{Van Ranst\}, Marc and Johan Neyts and Guy Baele and Piet Maes and Emmanuel Andr{\'e} and Simon Dellicour and \{Van Weyenbergh\}, Johan and \{COVID-19 Genomics Belgium Consortium\}",

note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = jun,

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

language = "English",

volume = "3",

pages = "722--733",

journal = "Nature Aging",

issn = "2662-8465",

publisher = "Nature Publishing Group",

number = "6",

}

Cuypers, L, Keyaerts, E, Hong, SL, Gorissen, S, Menezes, SM, Starick, M, Van Elslande, J, Weemaes, M, Wawina-Bokalanga, T, Marti-Carreras, J, Vanmechelen, B, Van Holm, B, Bloemen, M, Dogne, JM, Dufrasne, FE, Durkin, K, Ruelle, J, de Mendonca, R, Wollants, E, Vermeersch, P, Boulouffe, C, Djiena, A, Broucke, C, Catry, B, Lagrou, K, Van Ranst, M, Neyts, J, Baele, G, Maes, P, André, E, Dellicour, S, Van Weyenbergh, J & COVID-19 Genomics Belgium Consortium 2023, 'Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks', Nature Aging, vol. 3, no. 6, pp. 722-733. https://doi.org/10.1038/s43587-023-00421-1

TY - JOUR

T1 - Immunovirological and environmental screening reveals actionable risk factors for fatal COVID-19 during post-vaccination nursing home outbreaks

AU - Cuypers, Lize

AU - Keyaerts, Els

AU - Hong, Samuel Leandro

AU - Gorissen, Sarah

AU - Menezes, Soraya Maria

AU - Starick, Marick

AU - Van Elslande, Jan

AU - Weemaes, Matthias

AU - Wawina-Bokalanga, Tony

AU - Marti-Carreras, Joan

AU - Vanmechelen, Bert

AU - Van Holm, Bram

AU - Bloemen, Mandy

AU - Dogne, Jean Michel

AU - Dufrasne, François E.

AU - Durkin, Keith

AU - Ruelle, Jean

AU - de Mendonca, Ricardo

AU - Wollants, Elke

AU - Vermeersch, Pieter

AU - Wattiez, Ruddy

AU - Peeters, Michael

AU - Bakelants, Kate

AU - Denayer, Sarah

AU - Dufrasne, François E.

AU - Meex, Cécile

AU - Gillet, Laurent

AU - Artesi, Maria

AU - Hayette, Marie Pierre

AU - Bontems, Sébastien

AU - Bours, Vincent

AU - Gourzonès, Claire

AU - Ek, Olivier

AU - Bureau, Fabrice

AU - Kabamba, Benoit

AU - Gala, Jean Luc

AU - Bearzatto, Bertrand

AU - Ambroise, Jérôme

AU - Marchant, Arnaud

AU - Henin, Coralie

AU - Haerlingen, Benoit

AU - de Mendonca, Ricardo

AU - Delforge, Marie Luce

AU - Vael, Carl

AU - Berckmans, Lynsey

AU - Selhorst, Philippe

AU - Ariën, Kevin K.

AU - Van Dooren, Sonia

AU - Hinckel, Bruno

AU - Imamura, Hideo

AU - Janssen, Toon

AU - Caljon, Ben

AU - Soetens, Oriane

AU - Piérard, Denis

AU - Demuyser, Thomas

AU - Michel, Charlotte

AU - Vandenberg, Olivier

AU - van den Wijngaert, Sigi

AU - Zorzi, Giulia

AU - Van Lint, Philippe

AU - Verstrepen, Walter

AU - Naesens, Reinout

AU - Van Lent, Sarah

AU - Hilbert, Pascale

AU - Brohée, Sylvain

AU - Léonard, Pierre Emmanuel

AU - Karadurmus, Deniz

AU - Gras, Jeremie

AU - Féret, Damien

AU - Lambert, Barbara

AU - Vankeerberghen, Anne

AU - Holderbeke, Astrid

AU - De Beenhouwer, Hans

AU - Cattoir, Lien

AU - Lammens, Christine

AU - Xavier, Basil Britto

AU - Le Mercier, Marie

AU - Coppens, Jasmine

AU - Matheeussen, Veerle

AU - Goossens, Herman

AU - Martens, Geert A.

AU - Swaerts, Koen

AU - Van Hoecke, Frederik

AU - Desmet, Dieter

AU - Descheemaeker, Patrick

AU - Bogaerts, Pierre

AU - Degosserie, Jonathan

AU - Denis, Olivier

AU - Huang, Te Din

AU - Obbels, Dagmar

AU - Valgaeren, Hanne

AU - Frans, Johan

AU - Smismans, Annick

AU - Claus, Paul Emile

AU - Veltman, Denise

AU - Goegebuer, Truus

AU - Lemmens, Ann

AU - Van den Poel, Bea

AU - De Bock, Sonja

AU - Laffut, Wim

AU - Van Even, Ellen

AU - Van Acker, Jos

AU - Verfaillie, Charlotte

AU - Vanlaere, Elke

AU - De Rauw, Klara

AU - Waumans, Luc

AU - Van Meensel, Britt

AU - Cartuyvels, Reinoud

AU - Raymaekers, Marijke

AU - Verhasselt, Bruno

AU - Hellemans, Jorn

AU - Vanhee, Merijn

AU - Reynders, Marijke

AU - Boulouffe, Caroline

AU - Djiena, Achille

AU - Broucke, Caroline

AU - Catry, Boudewijn

AU - Lagrou, Katrien

AU - Van Ranst, Marc

AU - Neyts, Johan

AU - Baele, Guy

AU - Maes, Piet

AU - André, Emmanuel

AU - Dellicour, Simon

AU - Van Weyenbergh, Johan

AU - COVID-19 Genomics Belgium Consortium

PY - 2023/6

Y1 - 2023/6

N2 - 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.

AB - 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.

UR - https://www.scopus.com/pages/publications/85160051457

U2 - 10.1038/s43587-023-00421-1

DO - 10.1038/s43587-023-00421-1

M3 - Article

C2 - 37217661

AN - SCOPUS:85160051457

SN - 2662-8465

VL - 3

SP - 722

EP - 733

JO - Nature Aging

JF - Nature Aging

IS - 6

ER -

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

Abstract

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