Reduced Cortical Thickness Correlates of Cognitive Dysfunction in Post-COVID-19 Condition: Insights from a Long-Term Follow-up

References

1. 1.↵
   1. Ballering AV,
   2. van Zon SK,
   3. Olde Hartman TC, et al

   ; Lifelines Corona Research Initiative. Persistence of somatic symptoms after COVID-19 in the Netherlands: an observational cohort study. Lancet 2022;400:452–61 doi:10.1016/S0140-6736(22)01214-4 pmid:35934007

   CrossRefPubMed
2. 2.↵
   1. Perlis RH,
   2. Santillana M,
   3. Ognyanova K, et al

   . Prevalence and correlates of long COVID symptoms among US adults. JAMA Netw Open 2022;5:e2238804 doi:10.1001/jamanetworkopen.2022.38804 pmid:36301542

   CrossRefPubMed
3. 3.↵
   1. Bowe B,
   2. Xie Y,
   3. Al-Aly Z

   . Postacute sequelae of COVID-19 at 2 years. Nat Med 2023;29:2347–57 doi:10.1038/s41591-023-02521-2 pmid:37605079

   CrossRefPubMed
4. 4.↵
   1. Soriano JB,
   2. Murthy S,
   3. Marshall JC, et al

   ; WHO Clinical Case Definition Working Group on Post-COVID-19 Condition. A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect Dis 2021;22:e102–07 doi:10.1016/S1473-3099(21)00703-9 pmid:34951953

   CrossRefPubMed
5. 5.↵
   1. Davis HE,
   2. Assaf GS,
   3. McCorkell L, et al

   . Characterizing long COVID in an international cohort: 7 months of symptoms and their impact. EClinicalMedicine 2021;38:101019 doi:10.1016/j.eclinm.2021.101019 pmid:34308300

   CrossRefPubMed
6. 6.↵
   1. Bull-Otterson L,
   2. Baca S,
   3. Saydah S, et al

   . Post–COVID conditions among adult COVID-19 survivors aged 18–64 and ≥65 years—United States, March 2020–November 2021. MMWR Morb Mortal Wkly Rep 2022;71:713–17 doi:10.15585/mmwr.mm7121e1 pmid:36639608

   CrossRefPubMed
7. 7.↵
   1. Castanares-Zapatero D,
   2. Chalon P,
   3. Kohn L, et al

   . Pathophysiology and mechanism of long COVID: a comprehensive review. Ann Med 2022;54:1473–87 doi:10.1080/07853890.2022.2076901 pmid:35594336

   CrossRefPubMed
8. 8.↵
   1. Díez-Cirarda M,
   2. Yus M,
   3. Gómez-Ruiz N, et al

   . Multimodal neuroimaging in post-COVID syndrome and correlation with cognition. Brain 2023;146:2142–52 doi:10.1093/brain/awac384 pmid:36288544

   CrossRefPubMed
9. 9.
   1. Davis HE,
   2. McCorkell L,
   3. Vogel JM, et al

   . Long COVID: major findings, mechanisms and recommendations. Nat Rev Microbiol 2023;21:133–46 doi:10.1038/s41579-022-00846-2 pmid:36639608

   CrossRefPubMed
10. 10.↵
    1. Delgado-Alonso C,
    2. Valles-Salgado M,
    3. Delgado-Álvarez A, et al

    . Cognitive dysfunction associated with COVID-19: a comprehensive neuropsychological study. J Psychiatr Res 2022;150:40–46 doi:10.1016/j.jpsychires.2022.03.033 pmid:35349797

    CrossRefPubMed
11. 11.↵
    1. García‐Sánchez C,
    2. Calabria M,
    3. Gruden N, et al

    . Neuropsychological deficits in patients with cognitive complaints after COVID‐19. Brain Behav 2022;12:e508 doi:10.1002/brb3.2508 pmid:35137561

    CrossRefPubMed
12. 12.↵
    1. Voruz P,
    2. Allali G,
    3. Benzakour L, et al

    . Long COVID neuropsychological deficits after severe, moderate, or mild infection. Clinical and Translational Neuroscience 2022;6:9 doi:10.3390/ctn6020009

    CrossRef
13. 13.↵
    1. Hadad R,
    2. Khoury J,
    3. Stanger C, et al

    . Cognitive dysfunction following COVID-19 infection. J Neurovirol 2022;28:430–37 doi:10.1007/s13365-022-01079-y pmid:35618983

    CrossRefPubMed
14. 14.↵
    1. Ariza M,
    2. Cano N,
    3. Segura B, et al

    ; NAUTILUS Project Collaborative Group. COVID-19 severity is related to poor executive function in people with post-COVID conditions. J Neurol 2023;270:2392–408 doi:10.1007/s00415-023-11587-4 pmid:36939932

    CrossRefPubMed
15. 15.↵
    1. Douaud G,
    2. Lee S,
    3. Alfaro-Almagro F, et al

    . SARS-CoV-2 is associated with changes in brain structure in UK Biobank. Nature 2022;604:697–707 doi:10.1038/s41586-022-04569-5 pmid:35255491

    CrossRefPubMed
16. 16.↵
    1. Díez-Cirarda M,
    2. Yus-Fuertes M,
    3. Sanchez-Sanchez R, et al

    . Hippocampal subfield abnormalities and biomarkers of pathologic brain changes: from SARS-CoV-2 acute infection to post-COVID syndrome. eBioMedicine 2023;94:104711 doi:10.1016/j.ebiom.2023.104711 pmid:37453364

    CrossRefPubMed
17. 17.↵
    1. Lu Y,
    2. Li X,
    3. Geng D, et al

    . Cerebral micro-structural changes in COVID-19 patients: an MRI-based 3-month follow-up study. EClinicalMedicine 2020;25:100484 doi:10.1016/j.eclinm.2020.100484 pmid:32838240

    CrossRefPubMed
18. 18.↵
    1. Hafiz R,
    2. Gandhi TK,
    3. Mishra S, et al

    . Higher limbic and basal ganglia volumes in surviving COVID-negative patients and the relations to fatigue. Neuroimage Rep 2022;2:100095 doi:10.1016/j.ynirp.2022.100095 pmid:35496469

    CrossRefPubMed
19. 19.↵
    1. Qin Y,
    2. Wu J,
    3. Chen T, et al

    . Long-term microstructure and cerebral blood flow changes in patients recovered from COVID-19 without neurological manifestations. J Clin. Invest 2021;131:147329 doi:10.1172/JCI147329] pmid:33630760

    CrossRefPubMed
20. 20.↵
    1. Tu Y,
    2. Zhang Y,
    3. Li Y, et al

    . Post-traumatic stress symptoms in COVID-19 survivors: a self-report and brain imaging follow-up study. Mol Psychiatry 2021;26:7475–80 doi:10.1038/s41380-021-01223-w pmid:34285348

    CrossRefPubMed
21. 21.↵
    1. Heine J,
    2. Schwichtenberg K,
    3. Hartung TJ, et al

    . Structural brain changes in patients with post-COVID fatigue: a prospective observational study. EClinicalMedicine 2023;58:101874 doi:10.1016/j.eclinm.2023.101874 pmid:36873426

    CrossRefPubMed
22. 22.↵
    1. Rothstein TL

    . Cortical grey matter volume depletion links to neurological sequelae in post COVID-19 “long haulers.” BMC Neurol 2023;23:22 doi:10.1186/s12883-023-03049-1 pmid:36647063

    CrossRefPubMed
23. 23.↵
    1. Voruz P,
    2. Cionca A,
    3. Alcântra IJ, et al

    . Functional connectivity underlying cognitive and psychiatric symptoms in post-COVID-19 syndrome: is anosognosia a key determinant? Brain Commun 2022;4:fcac057 doi:10.1093/braincomms/fcac057 pmid:35350554

    CrossRefPubMed
24. 24.↵
    1. Cecchetti G,
    2. Agosta F,
    3. Canu E, et al

    . Cognitive, EEG, and MRI features of COVID-19 survivors: a 10-month study. J Neurol 2022;269:3400–12 doi:10.1007/s00415-022-11047-5 pmid:35249144

    CrossRefPubMed
25. 25.↵
    1. Bungenberg J,
    2. Humkamp K,
    3. Hohenfeld C, et al

    . Long COVID‐19: objectifying most self‐reported neurological symptoms. Ann Clin Transl Neurol 2022;9:141–54 doi:10.1002/acn3.51496 pmid:35060361

    CrossRefPubMed
26. 26.↵
    1. Hosp JA,
    2. Dressing A,
    3. Blazhenets G, et al

    . Cognitive impairment and altered cerebral glucose metabolism in the subacute stage of COVID-19. Brain 2021;144:1263–76 doi:10.1093/brain/awab009 pmid:33822001

    CrossRefPubMed
27. 27.↵
    1. Dacosta-Aguayo R,
    2. Lamonja-Vicente N,
    3. Chacón C, et al

    . Neurocognitive profile of the post-COVID condition in adults in Catalonia: a mixed method prospective cohort and nested case–control study: study protocol. Vaccines (Basel) 2022;10:849 doi:10.3390/vaccines10060849 pmid:35746457

    CrossRefPubMed
28. 28.↵
    World Health Organization. “A healthy lifestyle: WHO recommendations,” 06-May-2010. Available: https://www.who.int/europe/news-room/fact-sheets/item/a-healthy-lifestyle---who-recommendations. Accessed June 24, 2023
29. 29.↵
    1. Pena-Casanova J,
    2. Quinones-Ubeda S,
    3. Quintana-Aparicio M, et al

    ; for the NEURONORMA Study Team. Spanish Multicenter Normative Studies (NEURONORMA Project): Norms for Verbal Span, Visuospatial Span, Letter and Number Sequencing, Trail Making Test, and Symbol Digit Modalities Test. Arch Clin Neuropsychol 2009;24:321–41 doi:10.1093/arclin/acp038 pmid:19661109

    CrossRefPubMed
30. 30.↵
    1. Tamayo F,
    2. Casals-Coll M,
    3. Sánchez-Benavides G, et al

    . Estudios normativos españoles en población adulta joven (Proyecto NEURONORMA jóvenes): normas para las pruebas span verbal, span visuoespacial, Letter-Number Sequencing, Trail Making Test y Symbol Digit Modalities Test. Neurologia 2012;27:319–29 doi:10.1016/j.nrl.2011.12.020 pmid:22405214

    CrossRefPubMedWeb of Science
31. 31.↵
    1. Lezak MD,
    2. Howieson DB,
    3. Bigler ED, et al

    . Neuropsychological Assessment. 5th ed. Oxford University Press; 2012
32. 32.↵
    1. Pena-Casanova J,
    2. Quinones-Ubeda S,
    3. Gramunt-Fombuena N, et al

    ; for the NEURONORMA Study Team. Spanish multicenter normative studies (NEURONORMA Project): norms for verbal fluency tests. Arch. Clin. Neuropsychol 2009;24:395–411 doi:10.1093/arclin/acp042

    CrossRefPubMed
33. 33.↵
    1. Casals-Coll M,
    2. Sánchez-Benavides G,
    3. Quintana M, et al

    . Estudios normativos españoles en población adulta joven (proyecto NEURONORMA jóvenes): normas para los test de fluencia verbal. Neurología 2013;28:33–40 doi:10.1016/j.nrl.2012.02.010 pmid:19648583

    CrossRefPubMed
34. 34.↵
    1. Strauss E,
    2. Sherman E,
    3. Spreen O

    . A Compendium of Neuropsychological Tests: Adiministration, Norms, and Commentary. Oxford University Press; 2006
35. 35.↵
    1. Wechsler D

    . Wechsler Adult Intelligence Scale. WAIS-III. Pearson. 1997
36. 36.↵
    1. Schmidt M

    . Rey Auditory Verbal Learning Test: A Handbook. Los Angeles (CA): Western Psychological Services; 1996
37. 37.↵
    1. Pena-Casanova J,
    2. Gramunt-Fombuena N,
    3. Quinones-Ubeda S, et al

    ; for the NEURONORMA Study Team. Spanish Multicenter Normative Studies (NEURONORMA Project): norms for the Rey-Osterrieth Complex Figure (copy and memory), and Free and Cued Selective Reminding Test Arch Clin Neuropsychol 2009;24:371–93 doi:10.1093/arclin/acp041 pmid:19661107

    CrossRefPubMed
38. 38.↵
    1. Palomo R,
    2. Casals-Coll M,
    3. Sánchez-Benavides G, et al

    . Spanish normative studies in young adults (NEURONORMA young adults project): norms for the Rey-Osterrieth Complex Figure (copy and memory) and Free and Cued Selective Reminding Test Neurologia 2013;28:226–35 doi:10.1016/j.nrl.2012.03.008 pmid:22652140

    CrossRefPubMed
39. 39.↵
    1. Kaplan E,
    2. Goodglass H,
    3. Weintraub S

    . Boston Naming Test. Philadelpia: Lea & Febiger; 1983
40. 40.↵
    1. Strober LB,
    2. Bruce JM,
    3. Arnett PA, et al

    . Tired of not knowing what that fatigue score means? Normative data of the Modified Fatigue Impact Scale (MFIS). Mult Scler Relat Disord 2020;46:102576 doi:10.1016/j.msard.2020.102576 pmid:33296974

    CrossRefPubMed
41. 41.↵
    1. Gates TM,
    2. Cysique LA

    . The chronicity of HIV infection should drive the research strategy of NeuroHIV treatment studies: a critical review. CNS Drugs 2016;30:53–69 doi:10.1007/s40263-015-0302-7 pmid:26749584

    CrossRefPubMed
42. 42.↵
    1. Fischl B

    . FreeSurfer. Neuroimage 2012;62:774–81 doi:10.1016/j.neuroimage.2012.01.021 pmid:22248573

    CrossRefPubMedWeb of Science
43. 43.↵
    1. Winkler AM,
    2. Ridgway GR,
    3. Webster MA, et al

    . Permutation inference for the general linear model. Neuroimage 2014;92:381–97 doi:10.1016/j.neuroimage.2014.01.060 pmid:24530839

    CrossRefPubMed
44. 44.↵
    1. Taylor JR,
    2. Williams N,
    3. Cusack R, et al

    . The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) data repository: structural and functional MRI, MEG, and cognitive data from a cross-sectional adult lifespan sample. Neuroimage 2017;144:262–69 doi:10.1016/j.neuroimage.2015.09.018 pmid:26375206

    CrossRefPubMed
45. 45.↵
    1. Meiberth D,
    2. Scheef L,
    3. Wolfsgruber S, et al

    . Cortical thinning in individuals with subjective memory impairment. J Alzheimers Dis 2015;45:139–46 doi:10.3233/JAD-142322 pmid:25471190

    Abstract/FREE Full Text
46. 46.↵
    1. Krumm S,
    2. Kivisaari SL,
    3. Probst A, et al

    . Cortical thinning of parahippocampal subregions in very early Alzheimer’s disease. Neurobiol Aging 2016;38:188–96 doi:10.1016/j.neurobiolaging.2015.11.001 pmid:26827657

    CrossRefPubMed
47. 47.↵
    1. Sanabria-Diaz G,
    2. Etter MM,
    3. Melie-Garcia L, et al

    . Brain cortical alterations in COVID-19 patients with neurological symptoms. Front Neurosci 2022;16:992165 doi:10.3389/fnins.2022.992165 pmid:36340780

    CrossRefPubMed
48. 48.↵
    1. Petersen M,
    2. Nägele FL,
    3. Mayer C, et al

    . Brain imaging and neuropsychological assessment of individuals recovered from a mild to moderate SARS-CoV-2 infection. Proc Natl Acad Sci U S A 2023;120:e221732120 doi:10.1073/pnas.2217232120 pmid:3722027]5

    CrossRefPubMed
49. 49.↵
    1. Ferreira D,
    2. Molina Y,
    3. Machado A, et al

    . Cognitive decline is mediated by gray matter changes during middle age. Neurobiol Aging 2014;35:1086–94 doi:10.1016/j.neurobiolaging.2013.10.095 pmid:24239436

    CrossRefPubMed
50. 50.↵
    1. Josephs KA,
    2. Whitwell JL,
    3. Ahmed Z, et al

    . β-amyloid burden is not associated with rates of brain atrophy. Ann Neurol 2008;63:204–12 doi:10.1002/ana.21223 pmid:17894374

    CrossRefPubMedWeb of Science
51. 51.↵
    1. Sharma C,
    2. Bayry J

    . High risk of autoimmune diseases after COVID-19. Nat Rev Rheumatol 2023;19:399–400 doi:10.1038/s41584-023-00964-y pmid:37046064

    CrossRefPubMed
52. 52.↵
    1. Komaroff AL,
    2. Lipkin WI

    . Insights from myalgic encephalomyelitis/chronic fatigue syndrome may help unravel the pathogenesis of postacute COVID-19 syndrome. Trends Mol Med 2021;27:895–906 doi:10.1016/j.molmed.2021.06.002 pmid:34175230

    CrossRefPubMed
53. 53.↵
    1. Jason LA,
    2. Richman JA,
    3. Rademaker AW, et al

    . A community-based study of chronic fatigue syndrome. Arch Intern Med 1999;159:2129–37 doi:10.1001/archinte.159.18.2129 pmid:10527290

    CrossRefPubMedWeb of Science
54. 54.↵
    1. Thapaliya K,
    2. Marshall-Gradisnik S,
    3. Staines D, et al

    . Alteration of cortical volume and thickness in myalgic encephalomyelitis/chronic fatigue syndrome. Front Neurosci 2022;16:848730 doi:10.3389/fnins.2022.848730 pmid:35527811

    CrossRefPubMed
55. 55.↵
    1. Rebsamen M,
    2. Friedli C,
    3. Radojewski P, et al

    . Multiple sclerosis as a model to investigate SARS‐CoV effect on brain atrophy. CNS Neurosci Ther 2023;29:538–43 doi:10.1111/cns.14050 pmid:36479826

    CrossRefPubMed
56. 56.↵
    1. Fujimori J,
    2. Fujihara K,
    3. Wattjes M, et al

    . Patterns of cortical grey matter thickness reduction in multiple sclerosis. Brain Behav 2021;11:e02050 doi:10.1002/brb3.2050 pmid:33506628

    CrossRefPubMed
57. 57.↵
    1. Fernández-Castañeda A,
    2. Lu P,
    3. Geraghty AC, et al

    . Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation. Cell 2022;185:2452–68.e1668 doi:10.1016/j.cell.2022.06.008 pmid:35768006

    CrossRefPubMed
58. 58.↵
    1. Ghali A,
    2. Lacout C,
    3. Fortrat J-O, et al

    . Factors influencing the prognosis of patients with myalgic encephalomyelitis/chronic fatigue syndrome. Diagnostics 2022;12:2540 doi:10.3390/diagnostics12102540 pmid:36292229

    CrossRefPubMed
59. 59.↵
    1. Cauda F,
    2. Nani A,
    3. Manuello J, et al

    . Brain structural alterations are distributed following functional, anatomic and genetic connectivity. Brain 2018;141:3211–32 doi:10.1093/brain/awy252 pmid:30346490

    CrossRefPubMed