Post-acute COVID-19 neuropsychiatric symptoms are not associated with ongoing nervous system injury

Maxime Taquet; Zuzanna Skorniewska; Henrik Zetterberg; John R Geddes; Catherine J Mummery; James D Chalmers; Ling-Pei Ho; Alex Horsley; Michael Marks; Krisnah Poinasamy; Betty Raman; Olivia C Leavy; Matthew Richardson; Omer Elneima; Hamish J C McAuley; Aarti Shikotra; Amisha Singapuri; Marco Sereno; Ruth M Saunders; Victoria Claire Harris; Linzy Houchen-Wolloff; Parisa Mansoori; Neil J Greening; Ewen M Harrison; Annemarie B Docherty; Nazir I Lone; Jennifer Quint; William Greenhalf; Louise V Wain; Christopher E Brightling; Rachael E Evans; Paul J Harrison; Ivan Koychev; PHOSP-COVID Study Collaborative Group

doi:10.1093/braincomms/fcad357

Post-acute COVID-19 neuropsychiatric symptoms are not associated with ongoing nervous system injury

Brain Commun. 2023 Dec 27;6(1):fcad357. doi: 10.1093/braincomms/fcad357. eCollection 2024.

Authors

Maxime Taquet^{1

2}, Zuzanna Skorniewska¹, Henrik Zetterberg^{3

4

5

6

7

8}, John R Geddes^{1

2}, Catherine J Mummery⁵, James D Chalmers⁹, Ling-Pei Ho¹⁰, Alex Horsley^{11

12}, Michael Marks^{13

14

15}, Krisnah Poinasamy¹⁶, Betty Raman^{17

18}, Olivia C Leavy¹⁹, Matthew Richardson²⁰, Omer Elneima²⁰, Hamish J C McAuley²⁰, Aarti Shikotra²¹, Amisha Singapuri²⁰, Marco Sereno²⁰, Ruth M Saunders²⁰, Victoria Claire Harris^{20

22}, Linzy Houchen-Wolloff^{23

24

25}, Parisa Mansoori²⁶, Neil J Greening²⁰, Ewen M Harrison²⁷, Annemarie B Docherty²⁷, Nazir I Lone^{28

29}, Jennifer Quint³⁰, William Greenhalf^{31

32

33}, Louise V Wain^{19

20}, Christopher E Brightling²⁰, Rachael E Evans^{20

22}, Paul J Harrison^{1

2}, Ivan Koychev¹; PHOSP-COVID Study Collaborative Group

Collaborators

PHOSP-COVID Study Collaborative Group:
C E Brightling, R A Evans, L V Wain, J D Chalmers, V C Harris, L P Ho, A Horsley, M Marks, K Poinasamy, B Raman, A Shikotra, A Singapuri, C E Brightling, R A Evans, L V Wain, R Dowling, C Edwardson, O Elneima, S Finney, N J Greening, B Hargadon, V Harris, L Houchen-Wolloff, O C Leavy, H J C McAuley, C Overton, T Plekhanova, R M Saunders, M Sereno, A Singapuri, A Shikotra, C Taylor, S Terry, C Tong, B Zhao, D Lomas, E Sapey, C Berry, C E Bolton, N Brunskill, E R Chilvers, R Djukanovic, Y Ellis, D Forton, N French, J George, N A Hanley, N Hart, L McGarvey, N Maskell, H McShane, M Parkes, D Peckham, P Pfeffer, A Sayer, A Sheikh, A A R Thompson, N Williams, C E Brightling, W Greenhalf, M G Semple, M Ashworth, H E Hardwick, L Lavelle-Langham, W Reynolds, M Sereno, R M Saunders, A Singapuri, V Shaw, A Shikotra, B Venson, L V Wain, A B Docherty, E M Harrison, A Sheikh, J K Baillie, C E Brightling, L Daines, R Free, R A Evans, S Kerr, O C Leavy, N I Lone, H J C McAuley, R Pius, J Quint, M Richardson, M Sereno, M Thorpe, L V Wain, M Halling-Brown, F Gleeson, J Jacob, S Neubauer, B Raman, S Siddiqui, J M Wild, S Aslani, P Jezzard, H Lamlum, W Lilaonitkul, E Tunnicliffe, J Willoughby, L V Wain, J K Baillie, H Baxendale, C E Brightling, M Brown, J D Chalmers, R A Evans, B Gooptu, W Greenhalf, H E Hardwick, R G Jenkins, D Jones, I Koychev, C Langenberg, A Lawrie, P L Molyneaux, A Shikotra, J Pearl, M Ralser, N Sattar, R M Saunders, J T Scott, T Shaw, D Thomas, D Wilkinson, L G Heaney, A De Soyza, D Adeloye, C E Brightling, J S Brown, J Busby, J D Chalmers, C Echevarria, L Daines, O Elneima, R A Evans, J Hurst, P Novotny, P Pfeffer, K Poinasamy, J Quint, I Rudan, E Sapey, M Shankar-Hari, A Sheikh, S Siddiqui, S Walker, B Zheng, J R Geddes, M Hotopf, K Abel, R Ahmed, L Allan, C Armour, D Baguley, D Baldwin, C Ballard, K Bhui, G Breen, M Broome, T Brugha, E Bullmore, D Burn, F Callard, J Cavanagh, T Chalder, D Clark, A David, B Deakin, H Dobson, B Elliott, J Evans, R Francis, E Guthrie, P Harrison, M Henderson, A Hosseini, N Huneke, M Husain, T Jackson, I Jones, T Kabir, P Kitterick, A Korszun, I Koychev, J Kwan, A Lingford-Hughes, P Mansoori, H McAllister-Williams, K McIvor, L Milligan, R Morriss, E Mukaetova-Ladinska, K Munro, A Nevado-Holgado, T Nicholson, S Paddick, C Pariante, J Pimm, K Saunders, M Sharpe, G Simons, R Upthegrove, S Wessely, G P McCann, S Amoils, C Antoniades, A Banerjee, R Bell, A Bularga, C Berry, P Chowienczyk, J P Greenwood, A D Hughes, K Khunti, L Kingham, C Lawson, K Mangion, N L Mills, A J Moss, S Neubauer, B Raman, A N Sattar, C L Sudlow, M Toshner, P J M Openshaw, D Altmann, J K Baillie, R Batterham, H Baxendale, N Bishop, C E Brightling, P C Calder, R A Evans, J L Heeney, T Hussell, P Klenerman, J M Lord, P Moss, S L Rowland-Jones, W Schwaeble, M G Semple, R S Thwaites, L Turtle, L V Wain, S Walmsley, D Wraith, M J Rowland, A Rostron, J K Baillie, B Connolly, A B Docherty, N I Lone, D F McAuley, D Parekh, A Rostron, J Simpson, C Summers, R G Jenkins, J Porter, R J Allen, R Aul, J K Baillie, S Barratt, P Beirne, J Blaikley, R C Chambers, N Chaudhuri, C Coleman, E Denneny, L Fabbri, P M George, M Gibbons, F Gleeson, B Gooptu, B Guillen Guio, I Hall, N A Hanley, L P Ho, E Hufton, J Jacob, I Jarrold, G Jenkins, S Johnson, M G Jones, S Jones, F Khan, P Mehta, J Mitchell, P L Molyneaux, J E Pearl, K Piper Hanley, K Poinasamy, J Quint, D Parekh, P Rivera-Ortega, L C Saunders, M G Semple, J Simpson, D Smith, M Spears, L G Spencer, S Stanel, I Stewart, A A R Thompson, D Thickett, R Thwaites, L V Wain, S Walker, S Walsh, J M Wild, D G Wootton, L Wright, S Heller, M J Davies, H Atkins, S Bain, J Dennis, K Ismail, D Johnston, P Kar, K Khunti, C Langenberg, P McArdle, A McGovern, T Peto, J Petrie, E Robertson, N Sattar, K Shah, J Valabhji, B Young, L S Howard, Mark Toshner, C Berry, P Chowienczyk, D Lasserson, A Lawrie, O C Leavy, J Mitchell, L Price, J Quint, J Rossdale, N Sattar, C Sudlow, A A R Thompson, J M Wild, M Wilkins, S J Singh, W D-C Man, J M Lord, N J Greening, T Chalder, J T Scott, N Armstrong, E Baldry, M Baldwin, N Basu, M Beadsworth, L Bishop, C E Bolton, A Briggs, M Buch, G Carson, J Cavanagh, H Chinoy, E Daynes, S Defres, R A Evans, P Greenhaff, S Greenwood, M Harvie, M Husain, S MacDonald, A McArdle, H J C McAuley, A McMahon, M McNarry, C Nolan, K O'Donnell, D Parekh, J Pimm, J Sargent, L Sigfrid, M Steiner, D Stensel, A L Tan, J Whitney, D Wilkinson, D Wilson, M Witham, D G Wootton, T Yates, D Thomas, N Brunskill, S Francis, S Greenwood, C Laing, K Bramham, P Chowdhury, A Frankel, L Lightstone, S McAdoo, K McCafferty, M Ostermann, N Selby, C Sharpe, M Willicombe, A Shaw, L Armstrong, B Hairsine, H Henson, C Kurasz, L Shenton, S Fairbairn, A Dell, N Hawkings, J Haworth, M Hoare, A Lucey, V Lewis, G Mallison, H Nassa, C Pennington, A Price, C Price, A Storrie, G Willis, S Young, P Pfeffer, K Chong-James, C David, W Y James, A Martineau, O Zongo, A Sanderson, L G Heaney, C Armour, V Brown, T Craig, S Drain, B King, N Magee, D McAulay, E Major, L McGarvey, J McGinness, R Stone, A Haggar, A Bolger, F Davies, J Lewis, A Lloyd, R Manley, E McIvor, D Menzies, K Roberts, W Saxon, D Southern, C Subbe, V Whitehead, H El-Taweel, J Dawson, L Robinson, D Saralaya, L Brear, K Regan, K Storton, J Fuld, A Bermperi, I Cruz, K Dempsey, A Elmer, H Jones, S Jose, S Marciniak, M Parkes, C Ribeiro, J Taylor, M Toshner, L Watson, J Worsley, R Sabit, L Broad, A Buttress, T Evans, M Haynes, L Jones, L Knibbs, A McQueen, C Oliver, K Paradowski, J Williams, E Harris, C Sampson, C Lynch, E Davies, C Evenden, A Hancock, K Hancock, M Rees, L Roche, N Stroud, T Thomas-Woods, M Babores, J Bradley-Potts, M Holland, N Keenan, S Shashaa, H Wassall, E Beranova, H Weston, T Cosier, L Austin, J Deery, T Hazelton, C Price, H Ramos, R Solly, S Turney, L Pearce, W McCormack, S Pugmire, W Stoker, A Wilson, N Hart, L A Aguilar Jimenez, G Arbane, S Betts, K Bisnauthsing, A Dewar, P Chowdhury, A Dewar, G Kaltsakas, H Kerslake, M M Magtoto, P Marino, L M Martinez, M Ostermann, J Rossdale, T S Solano, E Wynn, N Williams, W Storrar, M Alvarez Corral, A Arias, E Bevan, D Griffin, J Martin, J Owen, S Payne, A Prabhu, A Reed, C Wrey Brown, C Lawson, T Burdett, J Featherstone, A Layton, C Mills, L Stephenson, N Easom, P Atkin, K Brindle, M G Crooks, K Drury, R Flockton, L Holdsworth, A Richards, D L Sykes, S Thackray-Nocera, C Wright, K E Lewis, A Mohamed, G Ross, S Coetzee, K Davies, R Hughes, R Loosley, L O'Brien, Z Omar, H McGuinness, E Perkins, J Phipps, A Taylor, H Tench, R Wolf-Roberts, L S Howard, O Kon, D C Thomas, S Anifowose, L Burden, E Calvelo, B Card, C Carr, E R Chilvers, D Copeland, P Cullinan, P Daly, L Evison, T Fayzan, H Gordon, S Haq, R G Jenkins, C King, K March, M Mariveles, L McLeavey, N Mohamed, S Moriera, U Munawar, J Nunag, U Nwanguma, L Orriss-Dib, A Ross, M Roy, E Russell, K Samuel, J Schronce, N Simpson, L Tarusan, C Wood, N Yasmin, R Reddy, A-M Guerdette, M Hewitt, K Warwick, S White, A M Shah, C J Jolley, O Adeyemi, R Adrego, H Assefa-Kebede, J Breeze, M Brown, S Byrne, T Chalder, P Dulawan, N Hart, A Hayday, A Hoare, A Knighton, M Malim, S Patale, I Peralta, N Powell, A Ramos, K Shevket, F Speranza, A Te, P Beirne, A Ashworth, J Clarke, C Coupland, M Dalton, E Wade, C Favager, J Greenwood, J Glossop, L Hall, T Hardy, A Humphries, J Murira, D Peckham, S Plein, J Rangeley, G Saalmink, A L Tan, B Whittam, N Window, J Woods, G Coakley, D G Wootton, L Turtle, L Allerton, A M All, M Beadsworth, A Berridge, J Brown, S Cooper, A Cross, S Defres, S L Dobson, J Earley, N French, W Greenhalf, H E Hardwick, K Hainey, J Hawkes, V Highett, S Kaprowska, A L Key, L Lavelle-Langham, N Lewis-Burke, G Madzamba, F Malein, S Marsh, C Mears, L Melling, M J Noonan, L Poll, J Pratt, E Richardson, A Rowe, M G Semple, V Shaw, K A Tripp, L O Wajero, S A Williams-Howard, J Wyles, S N Diwanji, P Papineni, S Gurram, S Quaid, G F Tiongson, E Watson, B Al-Sheklly, A Horsley, C Avram, J Blaikely, M Buch, N Choudhury, D Faluyi, T Felton, T Gorsuch, N A Hanley, T Hussell, Z Kausar, N Odell, R Osbourne, K Piper Hanley, K Radhakrishnan, S Stockdale, A De Soyza, C Echevarria, A Ayoub, J Brown, G Burns, G Davies, H Fisher, C Francis, A Greenhalgh, P Hogarth, J Hughes, K Jiwa, G Jones, G MacGowan, D Price, A Sayer, J Simpson, H Tedd, S Thomas, S West, M Witham, S Wright, A Young, M J McMahon, P Neill, D Anderson, H Bayes, C Berry, D Grieve, I B McInnes, N Basu, A Brown, A Dougherty, K Fallon, L Gilmour, K Mangion, A Morrow, K Scott, R Sykes, E K Sage, F Barrett, A Donaldson, M Patel, D Bell, A Brown, M Brown, R Hamil, K Leitch, L Macliver, J Quigley, A Smith, B Welsh, G Choudhury, J K Baillie, S Clohisey, A Deans, A B Docherty, J Furniss, E M Harrison, S Kelly, N I Lone, A Sheikh, J D Chalmers, D Connell, A Elliott, C Deas, J George, S Mohammed, J Rowland, A R Solstice, D Sutherland, C J Tee, B Jayaraman, T Light, C E Bolton, P Almeida, J Bonnington, M Chrystal, C Dupont, P Greenhaff, A Gupta, L Howard, W Jang, S Linford, L Matthews, R Needham, A Nikolaidis, S Prosper, K Shaw, A K Thomas, L P Ho, N M Rahman, M Ainsworth, A Alamoudi, A Bates, A Bloss, A Burns, P Carter, J Chen, F Conneh, T Dong, R I Evans, E Fraser, X Fu, J R Geddes, F Gleeson, P Harrison, M Havinden-Williams, P Jezzard, N Kanellakis, I Koychev, P Kurupati, X Li, H McShane, C Megson, K Motohashi, S Neubauer, D Nicoll, G Ogg, E Pacpaco, M Pavlides, Y Peng, N Petousi, N Rahman, B Raman, M J Rowland, K Saunders, M Sharpe, N Talbot, E Tunnicliffe, W D-C Man, B Patel, R E Barker, D Cristiano, N Dormand, M Gummadi, S Kon, K Liyanage, C M Nolan, S Patel, O Polgar, P Shah, S J Singh, J A Walsh, J Hurst, H Jarvis, S Mandal, S Ahmad, S Brill, L Lim, D Matila, O Olaosebikan, C Singh, M Toshner, H Baxendale, L Garner, C Johnson, J Mackie, A Michael, J Pack, K Paques, H Parfrey, J Parmar, N Diar Bakerly, P Dark, D Evans, E Hardy, A Harvey, D Holgate, S Knight, N Mairs, N Majeed, L McMorrow, J Oxton, J Pendlebury, C Summersgill, R Ugwuoke, S Whittaker, W Matimba-Mupaya, S Strong-Sheldrake, S L Rowland-Jones, A A R Thompson, J Bagshaw, M Begum, K Birchall, R Butcher, H Carborn, F Chan, K Chapman, Y Cheng, L Chetham, C Clark, Z Coburn, J Cole, M Dixon, A Fairman, J Finnigan, H Foot, D Foote, A Ford, R Gregory, K Harrington, L Haslam, L Hesselden, J Hockridge, A Holbourn, B Holroyd-Hind, L Holt, A Howell, E Hurditch, F Ilyas, C Jarman, A Lawrie, E Lee, J-H Lee, R Lenagh, A Lye, I Macharia, M Marshall, A Mbuyisa, J McNeill, S Megson, J Meiring, L Milner, S Misra, H Newell, T Newman, C Norman, L Nwafor, D Pattenadk, M Plowright, J Porter, P Ravencroft, C Roddis, J Rodger, P Saunders, J Sidebottom, J Smith, L Smith, N Steele, G Stephens, R Stimpson, B Thamu, N Tinker, K Turner, H Turton, P Wade, S Walker, J Watson, I Wilson, A Zawia, R Aul, M Ali, A Dunleavy, D Forton, N Msimanga, M Mencias, T Samakomva, S Siddique, J Teixeira, V Tavoukjian, J Hutchinson, L Allsop, K Bennett, P Buckley, M Flynn, M Gill, C Goodwin, M Greatorex, H Gregory, C Heeley, L Holloway, M Holmes, J Kirk, W Lovegrove, T A Sewell, S Shelton, D Sissons, K Slack, S Smith, D Sowter, S Turner, V Whitworth, I Wynter, L Warburton, S Painter, J Tomlinson, C Vickers, T Wainwright, D Redwood, J Tilley, S Palmer, G A Davies, L Connor, A Cook, T Rees, F Thaivalappil, C Thomas, A Butt, M Coulding, H Jones, S Kilroy, J McCormick, J McIntosh, H Savill, V Turner, J Vere, E Fraile, J Ugoji, S S Kon, H Lota, G Landers, M Nasseri, S Portukhay, A Hormis, A Daniels, J Ingham, L Zeidan, M Chablani, L Osborne, M Marks, J S Brown, N Ahwireng, B Bang, D Basire, R C Chambers, A Checkley, R Evans, M Heightman, T Hillman, J Hurst, J Jacob, S Janes, R Jastrub, M Lipman, S Logan, D Lomas, M Merida Morillas, H Plant, J C Porter, K Roy, E Wall, D Parekh, N Ahmad Haider, C Atkin, R Baggott, M Bates, A Botkai, A Casey, B Cooper, J Dasgin, K Draxlbauer, N Gautam, J Hazeldine, T Hiwot, S Holden, K Isaacs, T 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Woodhead, T Yates, A Yousuf, M G Jones, C Childs, R Djukanovic, S Fletcher, M Harvey, E Marouzet, B Marshall, R Samuel, T Sass, T Wallis, H Wheeler, R Dharmagunawardena, E Bright, P Crisp, M Stern, A Wight, L Bailey, A Reddington, A Ashish, J Cooper, E Robinson, A Broadley, K Howard, L Barman, C Brookes, K Elliott, L Griffiths, Z Guy, D Ionita, H Redfearn, C Sarginson, A Turnbull, Y Ellis, M Marks, A Briggs, K Holmes, Asthma Uk, British Lung, K Poinasamy, S Walker, M Halling-Brown, G Breen, M Hotopf, K Lewis, N Williams

Affiliations

¹ Department of Psychiatry, University of Oxford, Oxford OX3 7JX, UK.
² Oxford Health NHS Foundation Trust, Oxford OX3 7JX, UK.
³ Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, The Sahlgrenska Academy at the University of Gothenburg, Mölndal 413 90, Sweden.
⁴ Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal 413 90, Sweden.
⁵ Department of Neurodegenerative Disease, UCL Institute of Neurology, London WC1N 3BG, UK.
⁶ UK Dementia Research Institute at UCL, London WC1N 3BG, UK.
⁷ Hong Kong Center for Neurodegenerative Diseases, Hong Kong, China.
⁸ Wisconsin Alzheimer's Disease Research Center, University of Wisconsin School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53792, USA.
⁹ University of Dundee, Ninewells Hospital and Medical School, Dundee DD1 9SY, UK.
¹⁰ MRC Human Immunology Unit, University of Oxford, Oxford OX3 9DS, UK.
¹¹ Division of Infection, Immunity & Respiratory Medicine, Faculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PL, UK.
¹² Manchester University NHS Foundation Trust, Manchester M13 9WL, UK.
¹³ Department of Clinical Research, London School of Hygiene & Tropical Medicine, London WC1E 7HT, UK.
¹⁴ Hospital for Tropical Diseases, University College London Hospital, London WC1E 6JD, UK.
¹⁵ Division of Infection and Immunity, University College London, London WC1E 6BT, UK.
¹⁶ Asthma and Lung UK, London E1 8AA, UK.
¹⁷ Radcliffe Department of Medicine, University of Oxford, Oxford OX3 9DU, UK.
¹⁸ Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UK.
¹⁹ Department of Population Health Sciences, University of Leicester, Leicester LE1 7RH, UK.
²⁰ The Institute for Lung Health, NIHR Leicester Biomedical Research Centre, University of Leicester, Leicester LE3 9QP, UK.
²¹ NIHR Leicester Biomedical Research Centre, University of Leicester, Leicester LE5 4PW, UK.
²² University Hospitals of Leicester NHS Trust, Leicester LE5 4PW, UK.
²³ Centre for Exercise and Rehabilitation Science, NIHR Leicester Biomedical Research Centre-Respiratory, University of Leicester, Leicester LE5 4PW, UK.
²⁴ Department of Respiratory Sciences, University of Leicester, Leicester LE1 9HN, UK.
²⁵ Therapy Department, University Hospitals of Leicester, NHS Trust, Leicester LE5 4PW, UK.
²⁶ MQ: Transforming Mental Health, London EC1Y 0TH, UK.
²⁷ Centre for Medical Informatics, The Usher Institute, University of Edinburgh, Edinburgh EH16 4SS, UK.
²⁸ Usher Institute, University of Edinburgh, Edinburgh EH16 4SS, UK.
²⁹ Royal Infirmary of Edinburgh, NHS Lothian, Edinburgh EH16 4SA, UK.
³⁰ National Heart and Lung Institute, Imperial College London, London SW3 6LY, UK.
³¹ University of Liverpool, Liverpool L69 3BX, UK.
³² The CRUK Liverpool Experimental Cancer Medicine Centre, Liverpool L69 3GL, UK.
³³ Liverpool University Hospitals NHS Foundation Trust, Liverpool L7 8YE, UK.

Abstract

A proportion of patients infected with severe acute respiratory syndrome coronavirus 2 experience a range of neuropsychiatric symptoms months after infection, including cognitive deficits, depression and anxiety. The mechanisms underpinning such symptoms remain elusive. Recent research has demonstrated that nervous system injury can occur during COVID-19. Whether ongoing neural injury in the months after COVID-19 accounts for the ongoing or emergent neuropsychiatric symptoms is unclear. Within a large prospective cohort study of adult survivors who were hospitalized for severe acute respiratory syndrome coronavirus 2 infection, we analysed plasma markers of nervous system injury and astrocytic activation, measured 6 months post-infection: neurofilament light, glial fibrillary acidic protein and total tau protein. We assessed whether these markers were associated with the severity of the acute COVID-19 illness and with post-acute neuropsychiatric symptoms (as measured by the Patient Health Questionnaire for depression, the General Anxiety Disorder assessment for anxiety, the Montreal Cognitive Assessment for objective cognitive deficit and the cognitive items of the Patient Symptom Questionnaire for subjective cognitive deficit) at 6 months and 1 year post-hospital discharge from COVID-19. No robust associations were found between markers of nervous system injury and severity of acute COVID-19 (except for an association of small effect size between duration of admission and neurofilament light) nor with post-acute neuropsychiatric symptoms. These results suggest that ongoing neuropsychiatric symptoms are not due to ongoing neural injury.

Keywords: biomarkers; long COVID; neural injury.

Abstract

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