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Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Systematic Review Article

Imaging Markers of Neurologic Damage in COVID-19: A Systematic Review

Author(s): Sara Tavares Araújo, Clara Tavares Araújo, Rafael Silva e Castro, Lara Machado de Oliveira Brügger, Nathália Gualberto Souza e Silva, Debora Marques de Miranda and Ana Cristina Simões e Silva*

Volume 30, Issue 9, 2023

Published on: 21 September, 2022

Page: [1086 - 1106] Pages: 21

DOI: 10.2174/0929867329666220701124945

Price: $65

Abstract

Background and Objectives: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection commonly leads to neurologic manifestations. In the present review, we aimed to investigate potential neuroimaging markers of early diagnosis and prognosis of neurologic manifestations in COVID-19.

Methods: Our study was registered in the Prospective Register of Systematic Reviews (PROSPERO) under the protocol CDR42021265443. Based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, we selected 51 studies for whole-manuscript analysis.

Results: Magnetic resonance imaging (MRI) was the most common imaging method. The pattern, sites of lesion, signs, and symptoms of neurologic injury varied. Such manifestations possibly resulted from a direct viral infection or, most likely, from indirect mechanisms including coagulation disturbances, hypoxemia, and immunological responses.

Conclusion: The heterogeneity of the studies precludes any generalization of the findings. Brain MRI is the most informative imaging exam. Population studies, including the entire spectrum of COVID-19 are missing. There is still a need for future population studies evaluating neurologic manifestations of all COVID-19 severities acutely and chronically.

Keywords: Imaging, PET-CT, MRI, COVID-19, SARS-CoV-2, brain, neurologic.

[1]
Cutler, D.M.; Summers, L.H. The COVID-19 pandemic and the $16 trillion virus. JAMA, 2020, 324(15), 1495-1496.
[http://dx.doi.org/10.1001/jama.2020.19759] [PMID: 33044484]
[2]
Ellul, M.A.; Benjamin, L.; Singh, B.; Lant, S.; Michael, B.D.; Easton, A.; Kneen, R.; Defres, S.; Sejvar, J.; Solomon, T. Neurological associations of COVID-19. Lancet Neurol., 2020, 19(9), 767-783.
[http://dx.doi.org/10.1016/S1474-4422(20)30221-0] [PMID: 32622375]
[3]
Aggarwal, G.; Lippi, G.; Michael Henry, B. Cerebrovascular disease is associated with an increased disease severity in patients with Coronavirus Disease 2019 (COVID-19): A pooled analysis of published literature. Int. J. Stroke, 2020, 15(4), 385-389.
[http://dx.doi.org/10.1177/1747493020921664] [PMID: 32310015]
[4]
Maury, A.; Lyoubi, A.; Peiffer-Smadja, N.; de Broucker, T.; Meppiel, E. Neurological manifestations associated with SARS-CoV-2 and other coronaviruses: A narrative review for clinicians. Rev. Neurol. (Paris), 2021, 177(1-2), 51-64.
[http://dx.doi.org/10.1016/j.neurol.2020.10.001] [PMID: 33446327]
[5]
Zhou, F.; Yu, T.; Du, R.; Fan, G.; Liu, Y.; Liu, Z.; Xiang, J.; Wang, Y.; Song, B.; Gu, X.; Guan, L.; Wei, Y.; Li, H.; Wu, X.; Xu, J.; Tu, S.; Zhang, Y.; Chen, H.; Cao, B. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet, 2020, 395(10229), 1054-1062.
[http://dx.doi.org/10.1016/S0140-6736(20)30566-3] [PMID: 32171076]
[6]
Ruan, Q.; Yang, K.; Wang, W.; Jiang, L.; Song, J. Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med., 2020, 46(5), 846-848.
[http://dx.doi.org/10.1007/s00134-020-05991-x] [PMID: 32125452]
[7]
Woo, M. S.; Malsy, J.; Pöttgen, J.; Seddiq Zai, S.; Ufer, F.; Hadjilaou, A.; Schmiedel, S.; Addo, M. M.; Gerloff, C.; Heesen, C.; Schulze Zur Wiesch, J.; Friese, M. A. Frequent neurocognitive deficits after recovery from mild COVID-19. Brain Commun., 2020, 23(2), fcaa205.
[http://dx.doi.org/10.1093/braincomms/fcaa205]
[8]
Meinhardt, J.; Radke, J.; Dittmayer, C.; Franz, J.; Thomas, C.; Mothes, R.; Laue, M.; Schneider, J.; Brünink, S.; Greuel, S.; Lehmann, M.; Hassan, O.; Aschman, T.; Schumann, E.; Chua, R.L.; Conrad, C.; Eils, R.; Stenzel, W.; Windgassen, M.; Rößler, L.; Goebel, H-H.; Gelderblom, H.R.; Martin, H.; Nitsche, A.; Schulz-Schaeffer, W.J.; Hakroush, S.; Winkler, M.S.; Tampe, B.; Scheibe, F.; Körtvélyessy, P.; Reinhold, D.; Siegmund, B.; Kühl, A.A.; Elezkurtaj, S.; Horst, D.; Oesterhelweg, L.; Tsokos, M.; Ingold-Heppner, B.; Stadelmann, C.; Drosten, C.; Corman, V.M.; Radbruch, H.; Heppner, F.L. Olfactory transmucosal SARS-CoV-2 invasion as a port of central nervous system entry in individuals with COVID-19. Nat. Neurosci., 2021, 24(2), 168-175.
[http://dx.doi.org/10.1038/s41593-020-00758-5] [PMID: 33257876]
[9]
DeKosky, S.T.; Kochanek, P.M.; Valadka, A.B.; Clark, R.S.B.; Chou, S.H.-Y.; Au, A.K.; Horvat, C.; Jha, R.M.; Mannix, R.; Wisniewski, S.R.; Wintermark, M.; Rowell, S.E.; Welch, R.D.; Lewis, L.; House, S.; Tanzi, R.E.; Smith, D.R.; Vittor, A.Y.; Denslow, N.D.; Davis, M.D.; Glushakova, O.Y.; Hayes, R.L. Blood biomarkers for detection of brain injury in COVID-19 patients. J. Neurotrauma, 2021, 38(1), 1-43.
[http://dx.doi.org/10.1089/neu.2020.7332] [PMID: 33115334]
[10]
Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; Chou, R.; Glanville, J.; Grimshaw, J.M.; Hróbjartsson, A.; Lalu, M.M.; Li, T.; Loder, E.W.; Mayo-Wilson, E.; McDonald, S.; McGuinness, L.A.; Stewart, L.A.; Thomas, J.; Tricco, A.C.; Welch, V.A.; Whiting, P.; Moher, D. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 2021, 372(71), n71.
[http://dx.doi.org/10.1136/bmj.n71] [PMID: 33782057]
[11]
The ottawa hospital research institute. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (Accessed 2021 -12 -22).
[12]
Wells, G.A.; Shea, B.; O’Connell, D.; Peterson, J.; Welch, V.; Losos, M.; Tugwell, P. The newcastle-ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses; Oxford, 2000.
[13]
Herzog, R.; Álvarez-Pasquin, M.J.; Díaz, C.; Del Barrio, J.L.; Estrada, J.M.; Gil, Á. Are healthcare workers’ intentions to vaccinate related to their knowledge, beliefs and attitudes? A systematic review. BMC Public Health, 2013, 13, 154.
[http://dx.doi.org/10.1186/1471-2458-13-154] [PMID: 23421987]
[14]
Agarwal, S.; Jain, R.; Dogra, S.; Krieger, P.; Lewis, A.; Nguyen, V.; Melmed, K.; Galetta, S. Cerebral microbleeds and leukoencephalopathy in critically ill patients with COVID-19. Stroke, 2020, 51(9), 2649-2655.
[http://dx.doi.org/10.1161/STROKEAHA.120.030940] [PMID: 32755456]
[15]
Khedr, E.M.; Shoyb, A.; Mohammaden, M.; Saber, M. Acute symptomatic seizures and COVID-19: Hospital-based study. Epilepsy Res., 2021, 174, 106650.
[http://dx.doi.org/10.1016/j.eplepsyres.2021.106650] [PMID: 33993018]
[16]
Kremer, S.; Lersy, F.; Anheim, M.; Merdji, H.; Schenck, M.; Oesterlé, H.; Bolognini, F.; Messie, J.; Khalil, A.; Gaudemer, A.; Carré, S.; Alleg, M.; Lecocq, C.; Schmitt, E.; Anxionnat, R.; Zhu, F.; Jager, L.; Nesser, P.; Mba, Y.T.; Hmeydia, G.; Benzakoun, J.; Oppenheim, C.; Ferré, J-C.; Maamar, A.; Carsin-Nicol, B.; Comby, P-O.; Ricolfi, F.; Thouant, P.; Boutet, C.; Fabre, X.; Forestier, G.; de Beaurepaire, I.; Bornet, G.; Desal, H.; Boulouis, G.; Berge, J.; Kazémi, A.; Pyatigorskaya, N.; Lecler, A.; Saleme, S.; Edjlali-Goujon, M.; Kerleroux, B.; Constans, J-M.; Zorn, P-E.; Mathieu, M.; Baloglu, S.; Ardellier, F-D.; Willaume, T.; Brisset, J-C.; Caillard, S.; Collange, O.; Mertes, P.M.; Schneider, F.; Fafi-Kremer, S.; Ohana, M.; Meziani, F.; Meyer, N.; Helms, J.; Cotton, F. Neurologic and neuroimaging findings in patients with COVID-19: A retrospective multicenter study. Neurology, 2020, 95(13), e1868-e1882.
[http://dx.doi.org/10.1212/WNL.0000000000010112] [PMID: 32680942]
[17]
Naval-Baudin, P.; Rodriguez Caamaño, I.; Rubio-Maicas, C.; Pons-Escoda, A.; Fernández Viñas, M.M.; Nuñez, A.; Cardona, P.; Majos, C.; Cos, M.; Calvo, N. COVID-19 and ischemic stroke: Clinical and neuroimaging findings. J. Neuroimaging, 2021, 31(1), 62-66.
[http://dx.doi.org/10.1111/jon.12790] [PMID: 32986907]
[18]
Escalard, S.; Chalumeau, V.; Escalard, C.; Redjem, H.; Delvoye, F.; Hébert, S.; Smajda, S.; Ciccio, G.; Desilles, J-P.; Mazighi, M.; Blanc, R.; Maïer, B.; Piotin, M. Early brain imaging shows increased severity of acute ischemic strokes with large vessel occlusion in COVID-19 patients. Stroke, 2020, 51(11), 3366-3370.
[http://dx.doi.org/10.1161/STROKEAHA.120.031011] [PMID: 32813602]
[19]
Duan, K.; Premi, E.; Pilotto, A.; Cristillo, V.; Benussi, A.; Libri, I.; Giunta, M.; Bockholt, H.J.; Liu, J.; Campora, R.; Pezzini, A.; Gasparotti, R.; Magoni, M.; Padovani, A.; Calhoun, V.D. Alterations of frontal-temporal gray matter volume associate with clinical measures of older adults with COVID-19. Neurobiol. Stress, 2021, 14, 100326.
[http://dx.doi.org/10.1016/j.ynstr.2021.100326] [PMID: 33869679]
[20]
Virhammar, J.; Nääs, A.; Fällmar, D.; Cunningham, J.L.; Klang, A.; Ashton, N.J.; Jackmann, S.; Westman, G.; Frithiof, R.; Blennow, K.; Zetterberg, H.; Kumlien, E.; Rostami, E. Biomarkers for central nervous system injury in cerebrospinal fluid are elevated in COVID-19 and associated with neurological symptoms and disease severity. Eur. J. Neurol., 2021, 28(10), 3324-3331.
[http://dx.doi.org/10.1111/ene.14703] [PMID: 33369818]
[21]
Uginet, M.; Breville, G.; Hofmeister, J.; Machi, P.; Lalive, P.H.; Rosi, A.; Fitsiori, A.; Vargas, M.I.; Assal, F.; Allali, G.; Lovblad, K.-O. Cerebrovascular complications and vessel wall imaging in COVID-19 encephalopathy-a pilot study. Clin. Neuroradiol., 2021, 32, 287-293.
[http://dx.doi.org/10.1007/s00062-021-01008-2] [PMID: 33770199]
[22]
Aragao, M.F.V.V.; Leal, M.C.; Andrade, P.H.P.; Cartaxo Filho, O.Q.; Aragao, L.V.; Fonseca, T.M.; Valenca, M.A.; Leao, M.R.V.C.; Aragao, J.P.V.; Soares, M.L.; Lima, M.P.; Caldas, S.S.; Valenca, M.M. Clinical and radiological profiles of COVID-19 patients with neurological symptomatology: A comparative study. Viruses, 2021, 13(5), 845.
[http://dx.doi.org/10.3390/v13050845] [PMID: 34066524]
[23]
Caro-Domínguez, P.; Navallas, M.; Riaza-Martin, L.; Ghadimi Mahani, M.; Ugas Charcape, C.F.; Valverde, I.; D’Arco, F.; Toso, S.; Shelmerdine, S.C.; van Schuppen, J.; Secinaro, A.; Gräfe, D.; Camacho, M.; Neth, O.; Goo, H.W.; Kellenberger, C.J. Imaging findings of multisystem inflammatory syndrome in children associated with COVID-19. Pediatr. Radiol., 2021, 51(9), 1608-1620.
[http://dx.doi.org/10.1007/s00247-021-05065-0] [PMID: 33904952]
[24]
Chougar, L.; Shor, N.; Weiss, N.; Galanaud, D.; Leclercq, D.; Mathon, B.; Belkacem, S.; Ströer, S.; Burrel, S.; Boutolleau, D.; Demoule, A.; Rosso, C.; Delorme, C.; Seilhean, D.; Dormont, D.; Morawiec, E.; Raux, M.; Demeret, S.; Gerber, S.; Trunet, S.; Similowski, T.; Degos, V.; Rufat, P.; Corvol, J-C.; Lehéricy, S.; Pyatigorskaya, N. Retrospective observational study of brain MRI findings in patients with acute SARS-CoV-2 infection and neurologic manifestations. Radiology, 2020, 297(3), E313-E323.
[http://dx.doi.org/10.1148/radiol.2020202422] [PMID: 32677875]
[25]
Conklin, J.; Frosch, M.P.; Mukerji, S.S.; Rapalino, O.; Maher, M.D.; Schaefer, P.W.; Lev, M.H.; Gonzalez, R.G.; Das, S.; Champion, S.N.; Magdamo, C.; Sen, P.; Harrold, G.K.; Alabsi, H.; Normandin, E.; Shaw, B.; Lemieux, J.E.; Sabeti, P.C.; Branda, J.A.; Brown, E.N.; Westover, M.B.; Huang, S.Y.; Edlow, B.L. Susceptibility-weighted imaging reveals cerebral microvascular injury in severe COVID-19. J. Neurol. Sci., 2021, 421, 117308.
[http://dx.doi.org/10.1016/j.jns.2021.117308] [PMID: 33497950]
[26]
García-Moncó, J.C.; Cabrera-Muras, A.; Collía-Fernández, A.; Erburu-Iriarte, M.; Rodrigo-Armenteros, P.; Oyarzun-Irazu, I.; Martínez-Condor, D.; Bilbao-González, A.; Carmona-Abellán, M.; Caballero-Romero, I.; Gómez-Beldarrain, M. Neurological reasons for consultation and hospitalization during the COVID-19 pandemic. Neurol. Sci., 2020, 41(11), 3031-3038.
[http://dx.doi.org/10.1007/s10072-020-04714-w] [PMID: 32935157]
[27]
Guedj, E.; Campion, J.Y.; Dudouet, P.; Kaphan, E.; Bregeon, F.; Tissot-Dupont, H.; Guis, S.; Barthelemy, F.; Habert, P.; Ceccaldi, M.; Million, M.; Raoult, D.; Cammilleri, S.; Eldin, C. 18F-FDG brain PET hypometabolism in patients with long COVID. Eur. J. Nucl. Med. Mol. Imaging, 2021, 48(9), 2823-2833.
[http://dx.doi.org/10.1007/s00259-021-05215-4] [PMID: 33501506]
[28]
Helms, J.; Kremer, S.; Merdji, H.; Schenck, M.; Severac, F.; Clere-Jehl, R.; Studer, A.; Radosavljevic, M.; Kummerlen, C.; Monnier, A.; Boulay, C.; Fafi-Kremer, S.; Castelain, V.; Ohana, M.; Anheim, M.; Schneider, F.; Meziani, F. Delirium and encephalopathy in severe COVID-19: A cohort analysis of ICU patients. Crit. Care, 2020, 24(1), 491.
[http://dx.doi.org/10.1186/s13054-020-03200-1] [PMID: 32771053]
[29]
Kanberg, N.; Ashton, N.J.; Andersson, L-M.; Yilmaz, A.; Lindh, M.; Nilsson, S.; Price, R.W.; Blennow, K.; Zetterberg, H.; Gisslén, M. Neurochemical evidence of astrocytic and neuronal injury commonly found in COVID-19. Neurology, 2020, 95(12), e1754-e1759.
[http://dx.doi.org/10.1212/WNL.0000000000010111] [PMID: 32546655]
[30]
Kihira, S.; Schefflein, J.; Mahmoudi, K.; Rigney, B.; N Delman, B.; Mocco, J.; Doshi, A.; Belani, P. Association of coronavirus disease (COVID-19) with large vessel occlusion strokes: A case-control study. AJR Am. J. Roentgenol., 2021, 216(1), 150-156.
[http://dx.doi.org/10.2214/AJR.20.23847] [PMID: 32755225]
[31]
Kremer, S.; Lersy, F.; de Sèze, J.; Ferré, J.-C.; Maamar, A.; Carsin-Nicol, B.; Collange, O.; Bonneville, F.; Adam, G.; Martin-Blondel, G.; Rafiq, M.; Geeraerts, T.; Delamarre, L.; Grand, S.; Krainik, A.; Caillard, S.; Constans, J.M.; Metanbou, S.; Heintz, A.; Helms, J.; Schenck, M.; Lefèbvre, N.; Boutet, C.; Fabre, X.; Forestier, G.; de Beaurepaire, I.; Bornet, G.; Lacalm, A.; Oesterlé, H.; Bolognini, F.; Messié, J.; Hmeydia, G.; Benzakoun, J.; Oppenheim, C.; Bapst, B.; Megdiche, I.; Henry Feugeas, M.-C.; Khalil, A.; Gaudemer, A.; Jager, L.; Nesser, P.; Talla Mba, Y.; Hemmert, C.; Feuerstein, P.; Sebag, N.; Carré, S.; Alleg, M.; Lecocq, C.; Schmitt, E.; Anxionnat, R.; Zhu, F.; Comby, P.-O.; Ricolfi, F.; Thouant, P.; Desal, H.; Boulouis, G.; Berge, J.; Kazémi, A.; Pyatigorskaya, N.; Lecler, A.; Saleme, S.; Edjlali-Goujon, M.; Kerleroux, B.; Zorn, P-E.; Matthieu, M.; Baloglu, S.; Ardellier, F-D.; Willaume, T.; Brisset, J.C.; Boulay, C.; Mutschler, V.; Hansmann, Y.; Mertes, P.-M.; Schneider, F.; Fafi-Kremer, S.; Ohana, M.; Meziani, F.; David, J.-S.; Meyer, N.; Anheim, M.; Cotton, F. Brain MRI findings in severe COVID-19: A retrospective observational study. Radiology, 2020, 297(2), E242-E251.
[http://dx.doi.org/10.1148/radiol.2020202222] [PMID: 32544034]
[32]
Lersy, F.; Willaume, T.; Brisset, J-C.; Collange, O.; Helms, J.; Schneider, F.; Chammas, A.; Willaume, A.; Meyer, N.; Anheim, M.; Cotton, F.; Kremer, S. Critical illness-associated cerebral microbleeds for patients with severe COVID-19: Etiologic hypotheses. J. Neurol., 2021, 268(8), 2676-2684.
[http://dx.doi.org/10.1007/s00415-020-10313-8] [PMID: 33219827]
[33]
Rapalino, O.; Pourvaziri, A.; Maher, M.; Jaramillo-Cardoso, A.; Edlow, B.L.; Conklin, J.; Huang, S.; Westover, B.; Romero, J.M.; Halpern, E.; Gupta, R.; Pomerantz, S.; Schaefer, P.; Gonzalez, R.G.; Mukerji, S.S.; Lev, M.H. Clinical, imaging, and lab correlates of severe COVID-19 leukoencephalopathy. AJNR Am. J. Neuroradiol., 2021, 42(4), 632-638.
[http://dx.doi.org/10.3174/ajnr.A6966] [PMID: 33414226]
[34]
Hosp, J.A.; Dressing, A.; Blazhenets, G.; Bormann, T.; Rau, A.; Schwabenland, M.; Thurow, J.; Wagner, D.; Waller, C.; Niesen, W.D.; Frings, L.; Urbach, H.; Prinz, M.; Weiller, C.; Schroeter, N.; Meyer, P.T. Cognitive impairment and altered cerebral glucose metabolism in the subacute stage of COVID-19. Brain, 2021, 144(4), 1263-1276.
[http://dx.doi.org/10.1093/brain/awab009] [PMID: 33822001]
[35]
Pilotto, A.; Masciocchi, S.; Volonghi, I.; De Giuli, V.; Caprioli, F.; Mariotto, S.; Ferrari, S.; Bozzetti, S.; Imarisio, A.; Risi, B.; Premi, E.; Benussi, A.; Focà, E.; Castelli, F.; Zanusso, G.; Monaco, S.; Stefanelli, P.; Gasparotti, R.; Zekeridou, A.; McKeon, A.; Ashton, N.J.; BlennoW, K.; Zetterberg, H.; Padovani, A. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) encephalitis is a cytokine release syndrome: Evidences from cerebrospinal fluid analyses. Clin. Infect. Dis., 2021, 73(9), e3019-e3026.
[http://dx.doi.org/10.1093/cid/ciaa1933] [PMID: 33395482]
[36]
Meppiel, E.; Peiffer-Smadja, N.; Maury, A.; Bekri, I.; Delorme, C.; Desestret, V.; Gorza, L.; Hautecloque-Raysz, G.; Landre, S.; Lannuzel, A.; Moulin, S.; Perrin, P.; Petitgas, P.; SellaI, F.; Wang, A.; Tattevin, P.; de Broucker, T. Neurologic manifestations associated with COVID-19: A multicentre registry. Clin. Microbiol. Infect., 2021, 27(3), 458-466.
[http://dx.doi.org/10.1016/j.cmi.2020.11.005] [PMID: 33189873]
[37]
Petrescu, A-M.; Taussig, D.; Bouilleret, V. Electroencephalogram (EEG) in COVID-19: A systematic retrospective study. Neurophysiol. Clin., 2020, 50(3), 155-165.
[http://dx.doi.org/10.1016/j.neucli.2020.06.001] [PMID: 32653111]
[38]
Lin, L.; Al-Faraj, A.; Ayub, N.; Bravo, P.; Das, S.; Ferlini, L.; Karakis, I.; Lee, J.W.; Mukerji, S.S.; Newey, C.R.; Pathmanathan, J.; Abdennadher, M.; Casassa, C.; Gaspard, N.; Goldenholz, D.M.; Gilmore, E.J.; Jing, J.; Kim, J.A.; Kimchi, E.Y.; Ladha, H.S.; Tobochnik, S.; Zafar, S.; Hirsch, L.J.; Westover, M.B.; Shafi, M.M. Electroencephalographic abnormalities are common in COVID-19 and are associated with outcomes. Ann. Neurol., 2021, 89(5), 872-883.
[http://dx.doi.org/10.1002/ana.26060] [PMID: 33704826]
[39]
Khandwala, K.; Mubarak, F.; Ahmad, M.N. Imaging patterns of encephalopathy in patients with COVID-19. J. Coll. Physicians Surg. Pak., 2021, 30(1), S42-S45.
[http://dx.doi.org/10.29271/jcpsp.2021.01.S42] [PMID: 33650425]
[40]
Lambrecq, V.; Hanin, A.; Munoz-Musat, E.; Chougar, L.; Gassama, S.; Delorme, C.; Cousyn, L.; Borden, A.; Damiano, M.; Frazzini, V.; Huberfeld, G.; Landgraf, F.; Nguyen-Michel, V.-H.; Pichit, P.; Sangare, A.; Chavez, M.; Morélot-Panzini, C.; Morawiec, E.; Raux, M.; Luyt, C.-E.; Rufat, P.; Galanaud, D.; Corvol, J.-C.; Lubetzki, C.; Rohaut, B.; Demeret, S.; Pyatigorskaya, N.; Naccache, L.; Navarro, V. Association of clinical, biological, and brain magnetic resonance imaging findings with electroencephalographic findings for patients with COVID-19. JAMA Netw. Open, 2021, 4(3), e211489.
[http://dx.doi.org/10.1001/jamanetworkopen.2021.1489] [PMID: 33720371]
[41]
Mahammedi, A.; Ramos, A.; Bargalló, N.; Gaskill, M.; Kapur, S.; Saba, L.; Carrete, H., Jr; Sengupta, S.; Salvador, E.; Hilario, A.; Revilla, Y.; Sanchez, M.; Perez-Nuñez, M.; Bachir, S.; Zhang, B.; Oleaga, L.; Sergio, J.; Koren, L.; Martin-Medina, P.; Wang, L.; Benegas, M.; Ostos, F.; Gonzalez-Ortega, G.; Calleja, P.; Udstuen, G.; Williamson, B.; Khandwala, V.; Chadalavada, S.; Woo, D.; Vagal, A. Brain and lung imaging correlation in patients with COVID-19: Could the severity of lung disease reflect the prevalence of acute abnormalities on neuroimaging? A global multicenter observational study. AJNR Am. J. Neuroradiol., 2021, 42(6), 1008-1016.
[http://dx.doi.org/10.3174/ajnr.A7072] [PMID: 33707278]
[42]
Yoon, B.C.; Buch, K.; Lang, M.; Applewhite, B.P.; Li, M.D.; Mehan, W.A., Jr; Leslie-Mazwi, T.M.; Rincon, S.P. Clinical and neuroimaging correlation in patients with COVID-19. AJNR Am. J. Neuroradiol., 2020, 41(10), 1791-1796.
[http://dx.doi.org/10.3174/ajnr.A6717] [PMID: 32912875]
[43]
Lang, M.; Li, M.D.; Jiang, K.Z.; Yoon, B.C.; Mendoza, D.P.; Flores, E.J.; Rincon, S.P.; Mehan, W.A., Jr; Conklin, J.; Huang, S.Y.; Lang, A.L.; Giao, D.M.; Leslie-Mazwi, T.M.; Kalpathy-Cramer, J.; Little, B.P.; Buch, K. Severity of chest imaging is correlated with risk of acute neuroimaging findings among patients with COVID-19. AJNR Am. J. Neuroradiol., 2021, 42(5), 831-837.
[http://dx.doi.org/10.3174/ajnr.A7032] [PMID: 33541897]
[44]
Koh, J.S.; De Silva, D.A.; Quek, A.M.L.; Chiew, H.J.; Tu, T.M.; Seet, C.Y.H.; Hoe, R.H.M.; Saini, M.; Hui, A.C-F.; Angon, J.; Ker, J.R.; Yong, M.H.; Goh, Y.; Yu, W-Y.; Lim, T.C.C.; Tan, B.Y.Q.; Ng, K.W.P.; Yeo, L.L.L.; Pang, Y.Z.; Prakash, K.M.; Ahmad, A.; Thomas, T.; Lye, D.C.B.; Tan, K.; Umapathi, T. Neurology of COVID-19 in Singapore. J. Neurol. Sci., 2020, 418, 117118.
[http://dx.doi.org/10.1016/j.jns.2020.117118] [PMID: 32977228]
[45]
Rothstein, A.; Oldridge, O.; Schwennesen, H.; Do, D.; Cucchiara, B.L. Acute cerebrovascular events in hospitalized covid-19 patients. Stroke, 2020, 51(9), e219-e222.
[http://dx.doi.org/10.1161/STROKEAHA.120.030995] [PMID: 32684145]
[46]
Pilotto, A.; Masciocchi, S.; Volonghi, I.; Crabbio, M.; Magni, E.; De Giuli, V.; Caprioli, F.; Rifino, N.; Sessa, M.; Gennuso, M.; Cotelli, M.S.; Turla, M.; Balducci, U.; Mariotto, S.; Ferrari, S.; Ciccone, A.; Fiacco, F.; Imarisio, A.; Risi, B.; Benussi, A.; Premi, E.; Focà, E.; Caccuri, F.; Leonardi, M.; Gasparotti, R.; Castelli, F.; Zanusso, G.; Pezzini, A.; Padovani, A. Clinical presentation and outcomes of severe acute respiratory syndrome coronavirus 2-related encephalitis: The ENCOVID multicenter study. J. Infect. Dis., 2021, 223(1), 28-37.
[http://dx.doi.org/10.1093/infdis/jiaa609] [PMID: 32986824]
[47]
Lin, E.; Lantos, J.E.; Strauss, S.B.; Phillips, C.D.; Campion, T.R., Jr; Navi, B.B.; Parikh, N.S.; Merkler, A.E.; Mir, S.; Zhang, C.; Kamel, H.; Cusick, M.; Goyal, P.; Gupta, A. Brain imaging of patients with COVID-19: Findings at an Academic Institution during the Height of the Outbreak in New York City. AJNR Am. J. Neuroradiol., 2020, 41(11), 2001-2008.
[http://dx.doi.org/10.3174/ajnr.A6793] [PMID: 32819899]
[48]
Shahjouei, S.; Tsivgoulis, G.; Farahmand, G.; Koza, E.; Mowla, A.; Vafaei Sadr, A.; Kia, A.; Vaghefi Far, A.; Mondello, S.; Cernigliaro, A.; Ranta, A.; Punter, M.; Khodadadi, F.; Naderi, S.; Sabra, M.; Ramezani, M.; Amini Harandi, A.; Olulana, O.; Chaudhary, D.; Lyoubi, A.; Campbell, B.C.V.; Arenillas, J.F.; Bock, D.; Montaner, J.; Aghayari Sheikh Neshin, S.; Aguiar de Sousa, D.; Tenser, M.S.; Aires, A.; Alfonso, M.L.; Alizada, O.; Azevedo, E.; Goyal, N.; Babaeepour, Z.; Banihashemi, G.; Bonati, L.H.; Cereda, C.W.; Chang, J.J.; Crnjakovic, M.; De Marchis, G.M.; Del Sette, M.; Ebrahimzadeh, S.A.; Farhoudi, M.; Gandoglia, I.; Gonçalves, B.; Griessenauer, C.J.; Murat Hanci, M.; Katsanos, A.H.; Krogias, C.; Leker, R.R.; Lotman, L.; Mai, J.; Male, S.; Malhotra, K.; Malojcic, B.; Mesquita, T.; Mir Ghasemi, A.; Mohamed Aref, H.; Mohseni Afshar, Z.; Moon, J.; Niemelä, M.; Rezai Jahromi, B.; Nolan, L.; Pandhi, A.; Park, J.H.; Marto, J.P.; Purroy, F.; Ranji-Burachaloo, S.; Carreira, N.R.; Requena, M.; Rubiera, M.; Sajedi, S.A.; Sargento-Freitas, J.; Sharma, V.K.; Steiner, T.; Tempro, K.; Turc, G.; Ahmadzadeh, Y.; Almasi-Dooghaee, M.; Assarzadegan, F.; Babazadeh, A.; Baharvahdat, H.; Cardoso, F.B.; Dev, A.; Ghorbani, M.; Hamidi, A.; Hasheminejad, Z.S.; Hojjat-Anasri Komachali, S.; Khorvash, F.; Kobeissy, F.; Mirkarimi, H.; Mohammadi-Vosough, E.; Misra, D.; Noorian, A.R.; Nowrouzi-Sohrabi, P.; Paybast, S.; Poorsaadat, L.; Roozbeh, M.; Sabayan, B.; Salehizadeh, S.; Saberi, A.; Sepehrnia, M.; Vahabizad, F.; Yasuda, T.A.; Ghabaee, M.; Rahimian, N.; Harirchian, M.H.; Borhani-Haghighi, A.; Azarpazhooh, M.R.; Arora, R.; Ansari, S.; Avula, V.; Li, J.; Abedi, V.; Zand, R. SARS-CoV-2 and stroke characteristics: A report from the multinational COVID-19 stroke study group. Stroke, 2021, 52(5), e117-e130.
[http://dx.doi.org/10.1161/STROKEAHA.120.032927] [PMID: 33878892]
[49]
Mahammedi, A.; Saba, L.; Vagal, A.; Leali, M.; Rossi, A.; Gaskill, M.; Sengupta, S.; Zhang, B.; Carriero, A.; Bachir, S.; Crivelli, P.; Paschè, A.; Premi, E.; Padovani, A.; Gasparotti, R. Imaging of neurologic disease in hospitalized patients with COVID-19: An Italian multicenter retrospective observational study. Radiology, 2020, 297(2), E270-E273.
[http://dx.doi.org/10.1148/radiol.2020201933] [PMID: 32437313]
[50]
Lu, Y.; Li, X.; Geng, D.; Mei, N.; Wu, P-Y.; Huang, C-C.; Jia, T.; Zhao, Y.; Wang, D.; Xiao, A.; Yin, B. Cerebral micro-structural changes in COVID-19 patients - An MRI-based 3-month follow-up study. EClinicalMedicine, 2020, 25, 100484.
[http://dx.doi.org/10.1016/j.eclinm.2020.100484] [PMID: 32838240]
[51]
Lersy, F.; Anheim, M.; Willaume, T.; Chammas, A.; Brisset, J.-C.; Cotton, F.; Kremer, S. Cerebral vasculitis of medium-sized vessels as a possible mechanism of brain damage in COVID-19 patients. J. Neuroradiol., 2021, 48(3), 141-146.
[http://dx.doi.org/10.1016/j.neurad.2020.11.004] [PMID: 33340640]
[52]
Al-Mufti, F.; Amuluru, K.; Sahni, R.; Bekelis, K.; Karimi, R.; Ogulnick, J.; Cooper, J.; Overby, P.; Nuoman, R.; Tiwari, A.; Berekashvili, K.; Dangayach, N.; Liang, J.; Gupta, G.; Khandelwal, P.; Dominguez, J.F.; Sursal, T.; Kamal, H.; Dakay, K.; Taylor, B.; Gulko, E.; El-Ghanem, M.; Mayer, S.A.; Gandhi, C. Cerebral venous thrombosis in COVID-19: A New York Metropolitan cohort study. AJNR Am. J. Neuroradiol., 2021, 42(7), 1196-1200.
[http://dx.doi.org/10.3174/ajnr.A7134] [PMID: 33888450]
[53]
García-Azorín, D.; Abildúa, M.J.A.; Aguirre, M.E.E.; Fernández, S.F.; Moncó, J.C.G.; Guijarro-Castro, C.; Platas, M.G.; Delgado, F.R.; Andrés, J.M.L.; Ezpeleta, D. Neurological presentations of COVID-19: Findings from the spanish society of neurology neuro COVID-19 registry. J. Neurol. Sci., 2021, 423, 117283.
[http://dx.doi.org/10.1016/j.jns.2020.117283] [PMID: 33636661]
[54]
Jain, R.; Young, M.; Dogra, S.; Kennedy, H.; Nguyen, V.; Jones, S.; Bilaloglu, S.; Hochman, K.; Raz, E.; Galetta, S.; Horwtiz, L. COVID-19 related neuroimaging findings: A signal of thromboembolic complications and a strong prognostic marker of poor patient outcome. J. Neurol. Sci., 2020, 414, 116923.
[http://dx.doi.org/10.1016/j.jns.2020.116923] [PMID: 32447193]
[55]
Klironomos, S.; Tzortzakakis, A.; Kits, A.; Öhberg, C.; Kollia, E.; Ahoromazdae, A.; Almqvist, H.; Aspelin, Å.; Martin, H.; Ouellette, R.; Al-Saadi, J.; Hasselberg, M.; Haghgou, M.; Pedersen, M.; Petersson, S.; Finnsson, J.; Lundberg, J.; Falk Delgado, A.; Granberg, T. Nervous system involvement in coronavirus disease 2019: Results from a retrospective consecutive neuroimaging cohort. Radiology, 2020, 297(3), E324-E334.
[http://dx.doi.org/10.1148/radiol.2020202791] [PMID: 32729812]
[56]
Strauss, S.B.; Lantos, J.E.; Heier, L.A.; Shatzkes, D.R.; Phillips, C.D. Olfactory bulb signal abnormality in patients with COVID-19 WHO present with neurologic symptoms. AJNR Am. J. Neuroradiol., 2020, 41(10), 1882-1887.
[http://dx.doi.org/10.3174/ajnr.A6751] [PMID: 32855190]
[57]
Zeng, L.-K.; Zhu, H.-P.; Xiao, T.-T.; Peng, S.-C.; Yuan, W.-H.; Shao, J.-B.; Wang, L.-S.; Xiao, F.-F.; Xia, S.-W.; Lee, S.K.; Yan, K.; Zhou, W.-H. Short-term developmental outcomes in neonates born to mothers with COVID-19 from Wuhan, China. World J. Pediatr., 2021, 17(3), 253-262.
[http://dx.doi.org/10.1007/s12519-021-00426-z] [PMID: 33844176]
[58]
Yan, K.; Xiao, F.-F.; Jiang, Y.-W.; Xiao, T.-T.; Zhang, D.-J.; Yuan, W.-H.; Shao, J.-B.; Cheng, G.-Q.; Zeng, L.-K. Effects of SARS-CoV-2 infection on neuroimaging and neurobehavior in neonates. World J. Pediatr., 2021, 17(2), 171-179.
[http://dx.doi.org/10.1007/s12519-021-00423-2] [PMID: 33740237]
[59]
Requena, M.; Olivé-Gadea, M.; Muchada, M.; García-Tornel, Á.; Deck, M.; Juega, J.; Boned, S.; Rodríguez-Villatoro, N.; Piñana, C.; Pagola, J.; Rodríguez-Luna, D.; Hernández, D.; Rubiera, M.; Tomasello, A.; Molina, C.A.; Ribo, M. COVID-19 and stroke: Incidence and etiological description in a high-volume center. J. Stroke Cerebrovasc. Dis., 2020, 29(11), 105225.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2020.105225] [PMID: 33066917]
[60]
Agarwal, S.; Melmed, K.; Dogra, S.; Jain, R.; Conway, J.; Galetta, S.; Lewis, A. Increase in ventricle size and the evolution of white matter changes on serial imaging in critically Ill patients with COVID-19. Neurocrit. Care, 2021, 35(2), 491-500.
[http://dx.doi.org/10.1007/s12028-021-01207-2] [PMID: 33674942]
[61]
Khedr, E.M.; Soliman, R.K.; Abo-Elfetof, N.; Amin, M.; Mansour, O.Y.; Aly, A.; Zaki, A.F.; Saber, M. Clinical and radiological characteristics of acute cerebrovascular diseases among Egyptian patients with COVID-19 in Upper Egypt. Front. Neurol., 2021, 12, 635856.
[http://dx.doi.org/10.3389/fneur.2021.635856] [PMID: 33828521]
[62]
Sawlani, V.; Scotton, S.; Nader, K.; Jen, J.P.; Patel, M.; Gokani, K.; Denno, P.; Thaller, M.; Englezou, C.; Janjua, U.; Bowen, M.; Hoskote, C.; Veenith, T.; Hassan-Smith, G.; Jacob, S. COVID-19-related intracranial imaging findings: A large single-centre experience. Clin. Radiol., 2021, 76(2), 108-116.
[http://dx.doi.org/10.1016/j.crad.2020.09.002] [PMID: 33023738]
[63]
Tuma, R.L.; Guedes, B.F.; Carra, R.; Iepsen, B.; Rodrigues, J.; Camelo-Filho, A.E.; Kubota, G.; Ferrari, M.; Studart-Neto, A.; Oku, M.H.; Terrim, S.; Lopes, C.C.B.; Passos Neto, C.E.B.; Fiorentino, M.D.; Souza, J.C.C.; Baima, J.P.S.; Silva, T.; Perissinotti, I.; Martin, M.D.G.M.; Gonçalves, M.; Fortini, I.; Smid, J.; Adoni, T.; Lucato, L.; Nitrini, R.; Gomes, H.; Castro, L.H. Clinical, cerebrospinal fluid, and neuroimaging findings in COVID-19 encephalopathy: A case series. Neurol. Sci., 2021, 42(2), 479-489.
[http://dx.doi.org/10.1007/s10072-020-04946-w] [PMID: 33409828]

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