Top

Published in:

29-02-2024 | Post-COVID Syndrome | COVID-19

Post-COVID-19 conditions: a systematic review on advanced magnetic resonance neuroimaging findings

Authors: Sana Mohammadi, Sadegh Ghaderi

Published in: Neurological Sciences | Issue 5/2024

Abstract

Post-COVID conditions (PCCs) cover a wide spectrum of lingering symptoms experienced by survivors of coronavirus disease 2019 (COVID-19). Neurological and neuropsychiatric sequelae are common in PCCs. Advanced magnetic resonance imaging (MRI) techniques can reveal subtle alterations in brain structure, function, and perfusion that underlie these sequelae. This systematic review aimed to synthesize findings from studies that used advanced MRI to characterize brain changes in individuals with PCCs. A detailed literature search was conducted in the PubMed and Scopus databases to identify relevant studies that used advanced MRI modalities, such as structural MRI (sMRI), diffusion tensor imaging (DTI), functional MRI (fMRI), and perfusion-weighted imaging (PWI), to evaluate brain changes in PCCs. Twenty-five studies met the inclusion criteria, comprising 1219 participants with PCCs. The most consistent findings from sMRI were reduced gray matter volume (GMV) and cortical thickness (CTh) in cortical and subcortical regions. DTI frequently reveals increased mean diffusivity (MD), radial diffusivity (RD), and decreased fractional anisotropy (FA) in white matter tracts (WMTs) such as the corpus callosum, corona radiata, and superior longitudinal fasciculus. fMRI demonstrated altered functional connectivity (FC) within the default mode, salience, frontoparietal, somatomotor, subcortical, and cerebellar networks. PWI showed decreased cerebral blood flow (CBF) in the frontotemporal area, thalamus, and basal ganglia. Advanced MRI shows changes in the brain networks and regions of the PCCs, which may cause neurological and neuropsychiatric problems. Multimodal neuroimaging may help understand brain-behavior relationships. Longitudinal studies are necessary to better understand the progression of these brain anomalies.

Ghaderi S, Mohammadi S, Heidari M et al (2023) Post-COVID-19 Vaccination CNS magnetic resonance imaging findings: a systematic review. Can J Infect Dis Med Microbiol 2023:e1570830. https://doi.org/10.1155/2023/1570830CrossRef

Ghaderi S, Mohammadi S, Mohammadi M (2023) Obstructive sleep apnea and attention deficits: a systematic review of magnetic resonance imaging biomarkers and neuropsychological assessments. Brain Behav e3262. https://doi.org/10.1002/brb3.3262

Scholkmann F, May C-A (2023) COVID-19, post-acute COVID-19 syndrome (PACS, “long COVID”) and post-COVID-19 vaccination syndrome (PCVS, “post-COVIDvac-syndrome”): similarities and differences. Pathol Res Pract 246:154497. https://doi.org/10.1016/j.prp.2023.154497CrossRefPubMedPubMedCentral

Ajčević M, Iscra K, Furlanis G et al (2023) Cerebral hypoperfusion in post-COVID-19 cognitively impaired subjects revealed by arterial spin labeling MRI. Sci Rep 13:5808. https://doi.org/10.1038/s41598-023-32275-3CrossRefPubMedPubMedCentral

Rezaei N (2021) Coronavirus disease - COVID-19. Springer International Publishing, ChamCrossRef

Ghaznavi H, Elahimanesh F, Abdolmohammadi J, Mirzaie M, Ghaderi S (2022) Low-dose radiation therapy: a treatment for pneumonia resulting from COVID-19. J Radiother Pract 21(2):263–266. https://doi.org/10.1017/S1460396920001089

WHO Coronavirus (COVID-19) Dashboard. https://covid19.who.int. Accessed 11 Sep 2023

Wang Z, Yang L (2022) Post-acute sequelae of SARS-CoV-2 infection: a neglected public health issue. Front Public Health 10:908757. https://doi.org/10.3389/fpubh.2022.908757

Cooper E, Lound A, Atchison CJ et al (2023) Awareness and perceptions of long COVID among people in the REACT programme: early insights from a pilot interview study. PLoS ONE 18:e0280943. https://doi.org/10.1371/journal.pone.0280943CrossRefPubMedPubMedCentral

10.

Chippa V, Aleem A, Anjum F (2024) Post-acute coronavirus (COVID-19) syndrome. [Updated 2023 Feb 3]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. Available from: https://www.ncbi.nlm.nih.gov/books/NBK570608/

11.

Davis HE, McCorkell L, Vogel JM, Topol EJ (2023) Long COVID: major findings, mechanisms and recommendations. Nat Rev Microbiol 21:133–146. https://doi.org/10.1038/s41579-022-00846-2CrossRefPubMedPubMedCentral

12.

Bowe B, Xie Y, Al-Aly Z (2023) Postacute sequelae of COVID-19 at 2 years. Nat Med 1–11. https://doi.org/10.1038/s41591-023-02521-2

13.

Perumal R, Shunmugam L, Naidoo K et al (2023) Long COVID: a review and proposed visualization of the complexity of long COVID. Front Immunol 14:1117464. https://doi.org/10.3389/fimmu.2023.1117464CrossRefPubMedPubMedCentral

14.

Whitaker M, Elliott J, Chadeau-Hyam M et al (2022) Persistent COVID-19 symptoms in a community study of 606,434 people in England. Nat Commun 13:1957. https://doi.org/10.1038/s41467-022-29521-zCrossRefPubMedPubMedCentral

15.

Idehen JB, Kazi U, Quainoo-Acquah JA et al. On patterns of neuropsychiatric symptoms in patients with COVID-19: a systematic review of case reports. Cureus 14:e25004. https://doi.org/10.7759/cureus.25004

16.

Castanares-Zapatero D, Chalon P, Kohn L et al (2022) Pathophysiology and mechanism of long COVID: a comprehensive review. Ann Med 54:1473–1487. https://doi.org/10.1080/07853890.2022.2076901CrossRefPubMedPubMedCentral

17.

Monje M, Iwasaki A (2022) The neurobiology of long COVID. Neuron 110:3484–3496. https://doi.org/10.1016/j.neuron.2022.10.006CrossRefPubMedPubMedCentral

18.

Mohammadi M, Mohammadi S, Hadizadeh H et al (2023) Brain metastases from breast cancer using magnetic resonance imaging: a systematic review. J Med Radiat Sci. https://doi.org/10.1002/jmrs.715CrossRefPubMedPubMedCentral

19.

Mohammadi S, Ghaderi S (2023) Motor band sign in motor neuron diseases using magnetic resonance imaging: a systematic review. Acta Neurol Scand 2023:e6677967. https://doi.org/10.1155/2023/6677967CrossRef

20.

Huang S, Zhou Z, Yang D et al (2022) Persistent white matter changes in recovered COVID-19 patients at the 1-year follow-up. Brain 145:1830–1838. https://doi.org/10.1093/brain/awab435CrossRefPubMed

21.

Li R, Liu G, Zhang X et al (2023) Altered intrinsic brain activity and functional connectivity in COVID-19 hospitalized patients at 6-month follow-up. BMC Infect Dis 23:521. https://doi.org/10.1186/s12879-023-08331-8CrossRefPubMedPubMedCentral

22.

Latini F, Fahlström M, Fällmar D et al (2022) Can diffusion tensor imaging (DTI) outperform standard magnetic resonance imaging (MRI) investigations in post-COVID-19 autoimmune encephalitis? Ups J Med Sci 127:https://doi.org/10.48101/ujms.v127.8562. https://doi.org/10.48101/ujms.v127.8562

23.

Whitwell JL (2009) Voxel-based morphometry: an automated technique for assessing structural changes in the brain. J Neurosci 29:9661–9664. https://doi.org/10.1523/JNEUROSCI.2160-09.2009CrossRefPubMedPubMedCentral

24.

Han P, Stiller-Stut FP, Fjaeldstad A, Hummel T (2020) Greater hippocampal gray matter volume in subjective hyperosmia: a voxel-based morphometry study. Sci Rep 10:18869. https://doi.org/10.1038/s41598-020-75898-6CrossRefPubMedPubMedCentral

25.

Rusak F, Santa Cruz R, Lebrat L et al (2022) Quantifiable brain atrophy synthesis for benchmarking of cortical thickness estimation methods. Med Image Anal 82:102576. https://doi.org/10.1016/j.media.2022.102576CrossRefPubMed

26.

Bispo DD, Brandão PR, Pereira DA, Maluf FB, Dias BA, Paranhos HR, von Glehn F, de Oliveira AC, Regattieri NA, Silva LS, Yasuda CL (2022) Brain microstructural changes and fatigue after COVID-19. Front Neurol 13:1029302. https://doi.org/10.3389/fneur.2022.1029302

27.

Ghaderi S, Karami A, Ghalyanchi-Langeroudi A et al (2023) MRI findings in movement disorders and associated sleep disturbances. Am J Nucl Med Mol Imaging 13:77–94PubMedPubMedCentral

28.

Teller N, Chad JA, Wong A et al (2023) Feasibility of diffusion-tensor and correlated diffusion imaging for studying white-matter microstructural abnormalities: application in COVID-19. Hum Brain Mapp 44:3998–4010. https://doi.org/10.1002/hbm.26322CrossRefPubMedPubMedCentral

29.

Benedetti F, Palladini M, Paolini M et al (2021) Brain correlates of depression, post-traumatic distress, and inflammatory biomarkers in COVID-19 survivors: a multimodal magnetic resonance imaging study. Brain Behav Immun - Health 18:100387. https://doi.org/10.1016/j.bbih.2021.100387CrossRefPubMedPubMedCentral

30.

Zhang S, Li X, Lv J et al (2016) Characterizing and differentiating task-based and resting state FMRI signals via two-stage sparse representations. Brain Imaging Behav 10:21–32. https://doi.org/10.1007/s11682-015-9359-7CrossRefPubMedPubMedCentral

31.

Barnden L, Thapaliya K, Eaton-Fitch N, Barth M, Marshall-Gradisnik S (2023) Altered brain connectivity in long covid during cognitive exertion: a pilot study. Front Neurosci 17:1182607. https://doi.org/10.3389/fnins.2023.1182607

32.

Haitas N, Amiri M, Wilson M et al (2021) Age-preserved semantic memory and the CRUNCH effect manifested as differential semantic control networks: an fMRI study. PLoS ONE 16:e0249948. https://doi.org/10.1371/journal.pone.0249948CrossRefPubMedPubMedCentral

33.

Bakhshi SK, Quddusi A, Mahmood SD et al. Diagnostic implications of white matter tract involvement by intra-axial brain tumors. Cureus 13:e19355. https://doi.org/10.7759/cureus.19355

34.

Gerrish AC, Thomas AG, Dineen RA (2014) Brain white matter tracts: functional anatomy and clinical relevance. Semin Ultrasound CT MRI 35:432–444. https://doi.org/10.1053/j.sult.2014.06.003CrossRef

35.

Parente F, Colosimo A (2020) Functional connections between and within brain subnetworks under resting-state. Sci Rep 10:3438. https://doi.org/10.1038/s41598-020-60406-7CrossRefPubMedPubMedCentral

36.

Muccioli L, Sighinolfi G, Mitolo M et al (2023) Cognitive and functional connectivity impairment in post-COVID-19 olfactory dysfunction. Neuroimage Clin 38:103410. https://doi.org/10.1016/j.nicl.2023.103410CrossRefPubMedPubMedCentral

37.

Kim WSH, Ji X, Roudaia E et al (2022) MRI assessment of cerebral blood flow in nonhospitalized adults who self-isolated due to COVID-19. J Magn Reson Imaging. https://doi.org/10.1002/jmri.28555CrossRefPubMedPubMedCentral

38.

Qin Y, Wu J, Chen T et al (2021) Long-term microstructure and cerebral blood flow changes in patients recovered from COVID-19 without neurological manifestations. J Clin Invest 131(e147329):147329. https://doi.org/10.1172/JCI147329CrossRefPubMed

39.

Yus M, Matias-Guiu JA, Gil-Martínez L et al (2022) Persistent olfactory dysfunction after COVID-19 is associated with reduced perfusion in the frontal lobe. Acta Neurol Scand 146:194–198. https://doi.org/10.1111/ane.13627CrossRefPubMed

40.

Díez-Cirarda M, Yus M, Gómez-Ruiz N et al (2023) Multimodal neuroimaging in post-COVID syndrome and correlation with cognition. Brain 146:2142–2152. https://doi.org/10.1093/brain/awac384CrossRefPubMed

41.

Page MJ, McKenzie JE, Bossuyt PM et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71CrossRefPubMedPubMedCentral

42.

Wells, G., Shea, B., O’Connell, D., and Peterson, J. (2000). The Newcastle-Ottawa Scale (NOS) for assessing the quality of non-randomised studies in meta-analyses. Ottawa, on: Ottawa Hosp Res Inst. Available at: https://cir.nii.ac.jp/crid/1573950400281078528. Accessed 28 Feb 2024

43.

Lo CK-L, Mertz D, Loeb M (2014) Newcastle-Ottawa Scale: comparing reviewers’ to authors’ assessments. BMC Med Res Methodol 14:45. https://doi.org/10.1186/1471-2288-14-45CrossRefPubMedPubMedCentral

44.

Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605. https://doi.org/10.1007/s10654-010-9491-zCrossRefPubMed

45.

Recommendations for national SARS-CoV-2 testing strategies and diagnostic capacities. https://www.who.int/publications-detail-redirect/WHO-2019-nCoV-lab-testing-2021.1-eng. Accessed 18 Dec 2023

46.

Kamasak B, Ulcay T, Nisari M et al (2023) Effects of COVID-19 on brain and cerebellum: a voxel based morphometrical analysis. Bratisl Lek Listy 124:442–448. https://doi.org/10.4149/BLL_2023_068CrossRefPubMed

47.

Campabadal A, Oltra J, Junqué C et al (2023) Structural brain changes in post-acute COVID-19 patients with persistent olfactory dysfunction. Ann Clin Transl Neurol 10:195–203. https://doi.org/10.1002/acn3.51710CrossRefPubMed

48.

Rothstein TL (2023) Cortical Grey matter volume depletion links to neurological sequelae in post COVID-19 “long haulers.” BMC Neurol 23:22. https://doi.org/10.1186/s12883-023-03049-1CrossRefPubMedPubMedCentral

49.

Du Y, Zhao W, Huang S et al (2023) Two-year follow-up of brain structural changes in patients who recovered from COVID-19: a prospective study. Psychiatry Res 319:114969. https://doi.org/10.1016/j.psychres.2022.114969CrossRefPubMed

50.

Planchuelo-Gómez Á, García-Azorín D, Guerrero ÁL et al (2023) Structural brain changes in patients with persistent headache after COVID-19 resolution. J Neurol 270:13–31. https://doi.org/10.1007/s00415-022-11398-zCrossRefPubMed

51.

Besteher B, Machnik M, Troll M et al (2022) Larger gray matter volumes in neuropsychiatric long-COVID syndrome. Psychiatry Res 317:114836. https://doi.org/10.1016/j.psychres.2022.114836CrossRefPubMedPubMedCentral

52.

Esposito F, Cirillo M, De Micco R et al (2022) Olfactory loss and brain connectivity after COVID-19. Hum Brain Mapp 43:1548–1560. https://doi.org/10.1002/hbm.25741CrossRefPubMedPubMedCentral

53.

Yildirim D, Kandemirli SG, Tekcan Sanli DE et al (2022) A comparative olfactory MRI, DTI and fMRI study of COVID-19 related anosmia and post viral olfactory dysfunction. Acad Radiol 29:31–41. https://doi.org/10.1016/j.acra.2021.10.019CrossRefPubMed

54.

Lu Y, Li X, Geng D et al (2020) Cerebral micro-structural changes in COVID-19 patients - an MRI-based 3-month follow-up study. EClinicalMedicine 25:100484. https://doi.org/10.1016/j.eclinm.2020.100484CrossRefPubMedPubMedCentral

55.

Petersen M, Nägele FL, Mayer C et al (2023) Brain imaging and neuropsychological assessment of individuals recovered from a mild to moderate SARS-CoV-2 infection. Proc Natl Acad Sci U S A 120:e2217232120. https://doi.org/10.1073/pnas.2217232120CrossRefPubMedPubMedCentral

56.

Paolini M, Palladini M, Mazza MG et al (2023) Brain correlates of subjective cognitive complaints in COVID-19 survivors: a multimodal magnetic resonance imaging study. Eur Neuropsychopharmacol 68:1–10. https://doi.org/10.1016/j.euroneuro.2022.12.002CrossRefPubMed

57.

Huang S, Zhou X, Zhao W et al (2023) Dynamic white matter changes in recovered COVID-19 patients: a two-year follow-up study. Theranostics 13:724–735. https://doi.org/10.7150/thno.79902CrossRefPubMedPubMedCentral

58.

Catalogna M, Sasson E, Hadanny A et al (2022) Effects of hyperbaric oxygen therapy on functional and structural connectivity in post-COVID-19 condition patients: a randomized, sham-controlled trial. Neuroimage Clin 36:103218. https://doi.org/10.1016/j.nicl.2022.103218CrossRefPubMedPubMedCentral

59.

Yang L, Zhou M, Li L et al (2021) Characteristics of mental health implications and plasma metabolomics in patients recently recovered from COVID-19. Transl Psychiatry 11:307. https://doi.org/10.1038/s41398-021-01426-3CrossRefPubMedPubMedCentral

60.

Chang L, Ryan MC, Liang H et al (2023) Changes in brain activation patterns during working memory tasks in people with post-COVID condition and persistent neuropsychiatric symptoms. Neurology 100:e2409–e2423. https://doi.org/10.1212/WNL.0000000000207309CrossRefPubMed

61.

Voruz P, Cionca A, Jacot de Alcântara I et al (2023) Brain functional connectivity alterations associated with neuropsychological performance 6–9 months following SARS-CoV-2 infection. Hum Brain Mapp 44:1629–1646. https://doi.org/10.1002/hbm.26163CrossRefPubMed

62.

Harciarek M, Cosentino S (2013) Language, executive function and social cognition in the diagnosis of frontotemporal dementia syndromes. Int Rev Psychiatry 25:178–196. https://doi.org/10.3109/09540261.2013.763340CrossRefPubMedPubMedCentral

63.

Nowrangi MA, Lyketsos C, Rao V, Munro CA (2014) Systematic review of neuroimaging correlates of executive functioning: converging evidence from different clinical populations. J Neuropsychiatry Clin Neurosci 26:114–125. https://doi.org/10.1176/appi.neuropsych.12070176CrossRefPubMedPubMedCentral

64.

Narvacan K, Treit S, Camicioli R et al (2017) Evolution of deep gray matter volume across the human lifespan. Hum Brain Mapp 38:3771–3790. https://doi.org/10.1002/hbm.23604CrossRefPubMedPubMedCentral

65.

Chiu A, Fischbein N, Wintermark M et al (2021) COVID-19-induced anosmia associated with olfactory bulb atrophy. Neuroradiology 63:147–148. https://doi.org/10.1007/s00234-020-02554-1CrossRefPubMed

66.

Tai AP-L, Leung M-K, Lau BW-M et al (2023) Olfactory dysfunction: a plausible source of COVID-19-induced neuropsychiatric symptoms. Front Neurosci 17:1156914. https://doi.org/10.3389/fnins.2023.1156914CrossRefPubMedPubMedCentral

67.

Ghaderi S, Fatehi F, Kalra S, Batouli SAH (2023) MRI biomarkers for memory-related impairment in amyotrophic lateral sclerosis: a systematic review. Amyotroph Lateral Scler Frontotemporal Degeneration 0:1–17. https://doi.org/10.1080/21678421.2023.2236651CrossRef

68.

Aung WY, Mar S, Benzinger TL (2013) Diffusion tensor MRI as a biomarker in axonal and myelin damage. Imaging Med 5:427–440. https://doi.org/10.2217/iim.13.49CrossRefPubMedPubMedCentral

69.

Di Tella S, De Marco M, Baglio F, Silveri MC, Venneri A (2023) Resting-state functional connectivity is modulated by cognitive reserve in early Parkinson’s disease. Front Psychol 14:1207988. https://doi.org/10.3389/fpsyg.2023.1207988

70.

Catalino MP, Yao S, Green DL et al (2020) Mapping cognitive and emotional networks in neurosurgical patients using resting-state functional magnetic resonance imaging. Neurosurg Focus 48:E9. https://doi.org/10.3171/2019.11.FOCUS19773CrossRefPubMedPubMedCentral

71.

Huang H, Chen C, Rong B et al (2022) Resting-state functional connectivity of salience network in schizophrenia and depression. Sci Rep 12:11204. https://doi.org/10.1038/s41598-022-15489-9CrossRefPubMedPubMedCentral

72.

Keilholz S, Caballero-Gaudes C, Bandettini P et al (2017) Time-resolved resting-state functional magnetic resonance imaging analysis: current status, challenges, and new directions. Brain Connect 7:465–481. https://doi.org/10.1089/brain.2017.0543CrossRefPubMedPubMedCentral

73.

Ghaderi S, Olfati M, Ghaderi M et al (2023) Neurological manifestation in COVID-19 disease with neuroimaging studies. Am J Neurodegener Dis 12:42–84PubMedPubMedCentral

74.

Cascella M, De Blasio E (2022) Features and management of acute and chronic neuro-COVID. Springer International Publishing, ChamCrossRef

75.

Yadav SK, Kumar R, Macey PM et al (2013) Regional cerebral blood flow alterations in obstructive sleep apnea. Neurosci Lett 555:159–164. https://doi.org/10.1016/j.neulet.2013.09.033CrossRefPubMedPubMedCentral

76.

Yang Y, Xu H, Deng Z et al (2022) Functional connectivity and structural changes of thalamic subregions in episodic migraine. J Headache Pain 23:119. https://doi.org/10.1186/s10194-022-01491-zCrossRefPubMedPubMedCentral

77.

Vlaicu SI, Tatomir A, Cuevas J et al (2023) COVID, complement, and the brain. Front Immunol 14:1216457. https://doi.org/10.3389/fimmu.2023.1216457CrossRefPubMedPubMedCentral

Title: Post-COVID-19 conditions: a systematic review on advanced magnetic resonance neuroimaging findings
Authors: Sana Mohammadi
Sadegh Ghaderi
Publication date: 29-02-2024
Publisher: Springer International Publishing
Keywords: Post-COVID Syndrome
Smelling Disorder
Smelling Disorder
Magnetic Resonance Imaging
Magnetic Resonance Imaging
COVID-19
Published in: Neurological Sciences / Issue 5/2024
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-024-07427-6

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Post-COVID-19 conditions: a systematic review on advanced magnetic resonance neuroimaging findings

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2024

Long-term effects of vagus nerve stimulation therapy on cognitive functioning in patients with drug-resistant epilepsy

Virtual hospital and artificial intelligence: a first step towards the application of an innovative health system for the care of rare cerebrovascular diseases

Future treatment options for facial nerve palsy: a review on electrical stimulation devices for the orbicularis oculi muscle

Correlates and trajectories of relapses in relapsing–remitting multiple sclerosis

Exploring thrombus composition in cerebral venous thrombosis: the first case report with initial insights and implications for treatment advancements

Masitinib as a neuroprotective agent: a scoping review of preclinical and clinical evidence