Para-infectious brain injury in COVID-19 persists at follow-up despite attenuated cytokine and autoantibody responses

Michael, Benedict D.; Dunai, Cordelia; Needham, Edward J.; Tharmaratnam, Kukatharmini; Williams, Robyn; Huang, Yun; Boardman, Sarah A.; Clark, Jordan J.; Sharma, Parul; Subramaniam, Krishanthi; Wood, Greta K.; Collie, Ceryce; Digby, Richard; Ren, Alexander; Norton, Emma; Leibowitz, Maya; Ebrahimi, Soraya; Fower, Andrew; Fox, Hannah; Tato, Esteban; Ellul, Mark A.; Sunderland, Geraint; Held, Marie; Hetherington, Claire; Egbe, Franklyn N.; Palmos, Alish; Stirrups, Kathy; Grundmann, Alexander; Chiollaz, Anne-Cecile; Sanchez, Jean-Charles; Stewart, James P.; Griffiths, Michael; Solomon, Tom; Breen, Gerome; Coles, Alasdair J.; Kingston, Nathalie; Bradley, John R.; Chinnery, Patrick F.; Cavanagh, Jonathan; Irani, Sarosh R.; Vincent, Angela; Baillie, J. Kenneth; Openshaw, Peter J.; Semple, Malcolm G.; Taams, Leonie S.; Menon, David K.

Para-infectious brain injury in COVID-19 persists at follow-up despite attenuated cytokine and autoantibody responses

Benedict D. Michael (), Cordelia Dunai, Edward J. Needham, Kukatharmini Tharmaratnam, Robyn Williams, Yun Huang, Sarah A. Boardman, Jordan J. Clark, Parul Sharma, Krishanthi Subramaniam, Greta K. Wood, Ceryce Collie, Richard Digby, Alexander Ren, Emma Norton, Maya Leibowitz, Soraya Ebrahimi, Andrew Fower, Hannah Fox, Esteban Tato, Mark A. Ellul, Geraint Sunderland, Marie Held, Claire Hetherington, Franklyn N. Egbe, Alish Palmos, Kathy Stirrups, Alexander Grundmann, Anne-Cecile Chiollaz, Jean-Charles Sanchez, James P. Stewart, Michael Griffiths, Tom Solomon, Gerome Breen, Alasdair J. Coles, Nathalie Kingston, John R. Bradley, Patrick F. Chinnery, Jonathan Cavanagh, Sarosh R. Irani, Angela Vincent, J. Kenneth Baillie, Peter J. Openshaw, Malcolm G. Semple, Leonie S. Taams and David K. Menon
Additional contact information
Benedict D. Michael: University of Liverpool
Cordelia Dunai: University of Liverpool
Edward J. Needham: University of Cambridge
Kukatharmini Tharmaratnam: University of Liverpool
Robyn Williams: University of Oxford
Yun Huang: University of Liverpool
Sarah A. Boardman: University of Liverpool
Jordan J. Clark: University of Liverpool
Parul Sharma: University of Liverpool
Krishanthi Subramaniam: University of Liverpool
Greta K. Wood: University of Liverpool
Ceryce Collie: University of Liverpool
Richard Digby: University of Cambridge
Alexander Ren: University of Cambridge
Emma Norton: University of Cambridge
Maya Leibowitz: University of Cambridge
Soraya Ebrahimi: University of Cambridge
Andrew Fower: University of Oxford
Hannah Fox: University of Oxford
Esteban Tato: King’s College London
Mark A. Ellul: University of Liverpool
Geraint Sunderland: University of Liverpool
Marie Held: University of Liverpool
Claire Hetherington: University of Liverpool
Franklyn N. Egbe: University of Liverpool
Alish Palmos: King’s College London
Kathy Stirrups: Cambridge University Hospitals NHS Foundation
Alexander Grundmann: University of Southampton
Anne-Cecile Chiollaz: University of Geneva
Jean-Charles Sanchez: University of Geneva
James P. Stewart: University of Liverpool
Michael Griffiths: University of Liverpool
Tom Solomon: University of Liverpool
Gerome Breen: King’s College London
Alasdair J. Coles: University of Cambridge
Nathalie Kingston: Cambridge University Hospitals NHS Foundation
John R. Bradley: Cambridge University Hospitals NHS Foundation
Patrick F. Chinnery: University of Cambridge
Jonathan Cavanagh: University of Glasgow
Sarosh R. Irani: University of Oxford
Angela Vincent: University of Oxford
J. Kenneth Baillie: University of Edinburgh
Peter J. Openshaw: Imperial College London
Malcolm G. Semple: University of Liverpool
Leonie S. Taams: King’s College London
David K. Menon: University of Cambridge

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract To understand neurological complications of COVID-19 better both acutely and for recovery, we measured markers of brain injury, inflammatory mediators, and autoantibodies in 203 hospitalised participants; 111 with acute sera (1–11 days post-admission) and 92 convalescent sera (56 with COVID-19-associated neurological diagnoses). Here we show that compared to 60 uninfected controls, tTau, GFAP, NfL, and UCH-L1 are increased with COVID-19 infection at acute timepoints and NfL and GFAP are significantly higher in participants with neurological complications. Inflammatory mediators (IL-6, IL-12p40, HGF, M-CSF, CCL2, and IL-1RA) are associated with both altered consciousness and markers of brain injury. Autoantibodies are more common in COVID-19 than controls and some (including against MYL7, UCH-L1, and GRIN3B) are more frequent with altered consciousness. Additionally, convalescent participants with neurological complications show elevated GFAP and NfL, unrelated to attenuated systemic inflammatory mediators and to autoantibody responses. Overall, neurological complications of COVID-19 are associated with evidence of neuroglial injury in both acute and late disease and these correlate with dysregulated innate and adaptive immune responses acutely.

Date: 2023
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DOI: 10.1038/s41467-023-42320-4

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