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CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Review Article

Crosstalk between SARS-CoV-2 Infection and Neurological Disorders: A Review

Author(s): Asim Azhar*, Mohammad Akram Wali, Qudsia Rashid, Wajihul Hasan Khan, Khaled Al-hosaini, Mohammad Owais and Mohammad Amjad Kamal

Volume 22, Issue 5, 2023

Published on: 05 July, 2022

Page: [643 - 658] Pages: 16

DOI: 10.2174/1871527321666220418114009

Price: $65

Open Access Journals Promotions 2
Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent responsible for coronavirus disease (COVID-19), is an issue of global concern since March 2020. The respiratory manifestations of COVID-19 have widely been explained in the last couple of months of the pandemic. Initially, the virus was thought to be restricted to the pulmonary system; however, as time progressed and cases increased during the second wave of COVID-19, the virus affected other organs, including the nervous system. The neurological implication of SARS-CoV-2 infection is mounting, as substantiated by various reports, and in the majority of COVID-19 patients with neurological symptoms, the penetration of SARS-CoV-2 in the central nervous system (CNS) is likely. SARS-CoV-2 can enter the nervous system by exploiting the routes of olfactory mucosa, olfactory and sensory nerve endings, or endothelial and nerve tissues, thus crossing the neural-mucosal interface in the olfactory mucosa in the nose. Owing to multifactorial and complex pathogenic mechanisms, COVID-19 adds a large-scale risk to the entire nervous system. A thorough understanding of SARSCoV- 2 neurological damage is still vague; however, our comprehension of the virus is rapidly developing. The present comprehensive review will gain insights and provide neurological dimensions of COVID-19 and their associated anomalies. The review presents the entry routes of SARS-CoV-2 into the CNS to ascertain potential targets in the tissues owing to infection. We also discuss the molecular mechanisms involved, the array of clinical symptoms, and various nervous system diseases following the attack of SARS-CoV-2.

Keywords: ACE2, BBB, CNS, COVID-19, SARS-CoV-2, respiratory manifestations.

[1]
Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395(10223): 497-506.
[http://dx.doi.org/10.1016/S0140-6736(20)30183-5] [PMID: 31986264]
[2]
Conde Cardona G, Quintana Pájaro LD, Quintero Marzola ID, Ramos Villegas Y, Moscote Salazar LR. Neurotropism of SARS-CoV 2: Mechanisms and manifestations. J Neurol Sci 2020; 412: 116824.
[http://dx.doi.org/10.1016/j.jns.2020.116824] [PMID: 32299010]
[3]
Moriguchi T, Harii N, Goto J, et al. A first case of meningitis/encephalitis associated with SARS-Coronavirus-2. Int J Infect Dis 2020; 94: 55-8.
[http://dx.doi.org/10.1016/j.ijid.2020.03.062] [PMID: 32251791]
[4]
Mao L, Jin H, Wang M, et al. Neurologic manifestations of hospitalized patients with Coronavirus Disease 2019 in Wuhan, China. JAMA Neurol 2020; 77(6): 683-90.
[http://dx.doi.org/10.1001/jamaneurol.2020.1127] [PMID: 32275288]
[5]
Meinhardt J, Radke J, Dittmayer C, et al. Olfactory transmucosal SARS-CoV-2 invasion as a port of central nervous system entry in individuals with COVID-19. Nat Neurosci 2021; 24(2): 168-75.
[http://dx.doi.org/10.1038/s41593-020-00758-5] [PMID: 33257876]
[6]
Bradley BT, Bryan A. Emerging respiratory infections: The infectious disease pathology of SARS, MERS, pandemic influenza, and Legionella. Semin Diagn Pathol 2019; 36(3): 152-9.
[http://dx.doi.org/10.1053/j.semdp.2019.04.006] [PMID: 31054790]
[7]
Hui DSC, Zumla A. Severe acute respiratory syndrome: Historical, epidemiologic, and clinical features. Infect Dis Clin North Am 2019; 33(4): 869-89.
[http://dx.doi.org/10.1016/j.idc.2019.07.001] [PMID: 31668196]
[8]
Desforges M, Le Coupanec A, Dubeau P, et al. Human coronaviruses and other respiratory viruses: Underestimated opportunistic pathogens of the central nervous system? Viruses 2019; 12(1): E14.
[http://dx.doi.org/10.3390/v12010014] [PMID: 31861926]
[9]
Lau K-K, Yu W-C, Chu C-M, Lau S-T, Sheng B, Yuen K-Y. Possible central nervous system infection by SARS coronavirus. Emerg Infect Dis 2004; 10(2): 342-4.
[http://dx.doi.org/10.3201/eid1002.030638] [PMID: 15030709]
[10]
Li Y-C, Bai W-Z, Hashikawa T. The neuroinvasive potential of SARS-CoV2 may play a role in the respiratory failure of COVID-19 patients. J Med Virol 2020; 92(6): 552-5.
[http://dx.doi.org/10.1002/jmv.25728] [PMID: 32104915]
[11]
Li Y, Li M, Wang M, et al. Acute cerebrovascular disease following COVID-19: A single center, retrospective, observational study. Stroke Vasc Neurol 2020; 5(3): 279-84.
[http://dx.doi.org/10.1136/svn-2020-000431] [PMID: 32616524]
[12]
Karimi N, Sharifi Razavi A, Rouhani N. Frequent convulsive seizures in an adult patient with COVID-19: A case report. Iran Red Crescent Med J 2020; 22(3): 102828.
[http://dx.doi.org/10.5812/ircmj.102828]
[13]
Zhao H, Shen D, Zhou H, Liu J, Chen S. Guillain-Barré syndrome associated with SARS-CoV-2 infection: Causality or coincidence? Lancet Neurol 2020; 19(5): 383-4.
[http://dx.doi.org/10.1016/S1474-4422(20)30109-5] [PMID: 32246917]
[14]
Zhao K, Huang J, Dai D, Feng Y, Liu L, Nie S. Acute myelitis after SARS-CoV-2 infection: A case report Neurology 2020; 2020: 20035105.
[http://dx.doi.org/10.1101/2020.03.16.20035105]
[15]
Poyiadji N, Shahin G, Noujaim D, Stone M, Patel S, Griffith B. COVID-19-associated acute hemorrhagic necrotizing encephalopathy: Imaging features. Radiology 2020; 296(2): E119-20.
[http://dx.doi.org/10.1148/radiol.2020201187] [PMID: 32228363]
[16]
Sedaghat Z, Karimi N. Guillain Barre syndrome associated with COVID-19 infection: A case report. J Clin Neurosci 2020; 76: 233-5.
[http://dx.doi.org/10.1016/j.jocn.2020.04.062] [PMID: 32312628]
[17]
Solomon IH, Normandin E, Bhattacharyya S, et al. Neuropathological features of Covid-19. N Engl J Med 2020; 383(10): 989-92.
[http://dx.doi.org/10.1056/NEJMc2019373] [PMID: 32530583]
[18]
van Riel D, Verdijk R, Kuiken T. The olfactory nerve: A shortcut for influenza and other viral diseases into the central nervous system. J Pathol 2015; 235(2): 277-87.
[http://dx.doi.org/10.1002/path.4461] [PMID: 25294743]
[19]
Wu F, Zhao S, Yu B, et al. A new coronavirus associated with human respiratory disease in China. Nature 2020; 579(7798): 265-9.
[http://dx.doi.org/10.1038/s41586-020-2008-3] [PMID: 32015508]
[20]
Zhou P, Yang X-L, Wang X-G, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020; 579(7798): 270-3.
[http://dx.doi.org/10.1038/s41586-020-2012-7] [PMID: 32015507]
[21]
Zhu N, Zhang D, Wang W, et al. China Novel Coronavirus Investigating and Research Team. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med 2020; 382(8): 727-33.
[http://dx.doi.org/10.1056/NEJMoa2001017] [PMID: 31978945]
[22]
Coronaviridae Study Group of the International Committee on Taxonomy of Viruses. The species severe acute respiratory syndrome-related coronavirus: Classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol 2020; 5(4): 536-44.
[http://dx.doi.org/10.1038/s41564-020-0695-z] [PMID: 32123347]
[23]
Tang X, Wu C, Li X, et al. On the origin and continuing evolution of SARS-CoV-2. Natl Sci Rev 2020; 7(6): 1012-23.
[http://dx.doi.org/10.1093/nsr/nwaa036] [PMID: 34676127]
[24]
Cao C, Cai Z, Xiao X, et al. The architecture of the SARS-CoV-2 RNA genome inside virion. Nat Commun 2021; 12(1): 3917.
[http://dx.doi.org/10.1038/s41467-021-22785-x] [PMID: 34168138]
[25]
Andersen KG, Rambaut A, Lipkin WI, Holmes EC, Garry RF. The proximal origin of SARS-CoV-2. Nat Med 2020; 26(4): 450-2.
[http://dx.doi.org/10.1038/s41591-020-0820-9] [PMID: 32284615]
[26]
Azhar A, Al-hosaini K, Khan PA, et al. Promiscuous biological features of newly emerged SARS-CoV-2 facilitate its unrestrained outbreak: An update. Coronaviruses 2021; 02(10): e170821191027.
[http://dx.doi.org/10.2174/2666796702666210202125638]
[27]
Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020; 181(2): 271-280.e8.
[http://dx.doi.org/10.1016/j.cell.2020.02.052] [PMID: 32142651]
[28]
Netland J, Meyerholz DK, Moore S, Cassell M, Perlman S. Severe acute respiratory syndrome coronavirus infection causes neuronal death in the absence of encephalitis in mice transgenic for human ACE2. J Virol 2008; 82(15): 7264-75.
[http://dx.doi.org/10.1128/JVI.00737-08] [PMID: 18495771]
[29]
Doobay MF, Talman LS, Obr TD, Tian X, Davisson RL, Lazartigues E. Differential expression of neuronal ACE2 in transgenic mice with overexpression of the brain renin-angiotensin system. Am J Physiol Regul Integr Comp Physiol 2007; 292(1): R373-81.
[http://dx.doi.org/10.1152/ajpregu.00292.2006] [PMID: 16946085]
[30]
Khan S, Gomes J. Neuropathogenesis of SARS-CoV-2 infection. eLife 2020; 9: e59136.
[http://dx.doi.org/10.7554/eLife.59136] [PMID: 32729463]
[31]
Brann DH, Tsukahara T, Weinreb C, et al. Non-neuronal expression of SARS-CoV-2 entry genes in the olfactory system suggests mechanisms underlying COVID-19-associated anosmia. Sci Adv 2020; 6(31): eabc5801.
[http://dx.doi.org/10.1126/sciadv.abc5801] [PMID: 32937591]
[32]
Hu Z, Song C, Xu C, et al. Clinical characteristics of 24 asymptomatic infections with COVID-19 screened among close contacts in Nanjing, China. Sci China Life Sci 2020; 63(5): 706-11.
[http://dx.doi.org/10.1007/s11427-020-1661-4] [PMID: 32146694]
[33]
Jamil S, Mark N, Carlos G, Cruz CSD, Gross JE, Pasnick S. Diagnosis and management of COVID-19 disease. Am J Respir Crit Care Med 2020; 201(10): 19-P20.
[http://dx.doi.org/10.1164/rccm.2020C1] [PMID: 32223716]
[34]
Guan W-J, Ni Z-Y, Hu Y, et al. China Medical Treatment Expert Group for Covid-19. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020; 382(18): 1708-20.
[http://dx.doi.org/10.1056/NEJMoa2002032] [PMID: 32109013]
[35]
Desai AN, Patel P. Stopping the spread of COVID-19. JAMA 2020; 323(15): 1516.
[http://dx.doi.org/10.1001/jama.2020.4269] [PMID: 32196079]
[36]
Chen J. Pathogenicity and transmissibility of 2019-nCoV-A quick overview and comparison with other emerging viruses. Microbes Infect 2020; 22(2): 69-71.
[http://dx.doi.org/10.1016/j.micinf.2020.01.004] [PMID: 32032682]
[37]
Sanche S, Lin YT, Xu C, Romero-Severson E, Hengartner N, Ke R. High contagiousness and rapid spread of severe acute respiratory syndrome coronavirus 2. Emerg Infect Dis 2020; 26(7): 1470-7.
[http://dx.doi.org/10.3201/eid2607.200282] [PMID: 32255761]
[38]
Li F. Structure, function, and evolution of coronavirus spike proteins. Annu Rev Virol 2016; 3(1): 237-61.
[http://dx.doi.org/10.1146/annurev-virology-110615-042301] [PMID: 27578435]
[39]
Tan HW, Xu Y-M, Lau ATY. Angiotensin-converting enzyme 2: The old door for new severe acute respiratory syndrome coronavirus 2 infection. Rev Med Virol 2020; 30(5): e2122.
[http://dx.doi.org/10.1002/rmv.2122] [PMID: 32602627]
[40]
Shang J, Ye G, Shi K, et al. Structural basis of receptor recognition by SARS-CoV-2. Nature 2020; 581(7807): 221-4.
[http://dx.doi.org/10.1038/s41586-020-2179-y] [PMID: 32225175]
[41]
Simmons G, Gosalia DN, Rennekamp AJ, Reeves JD, Diamond SL, Bates P. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci USA 2005; 102(33): 11876-81.
[http://dx.doi.org/10.1073/pnas.0505577102] [PMID: 16081529]
[42]
Hamming I, Timens W, Bulthuis ML, Lely AT, Navis G, van Goor H. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J Pathol 2004; 203(2): 631-7.
[http://dx.doi.org/10.1002/path.1570] [PMID: 15141377]
[43]
He L, Mäe MA, Muhl L, et al. Pericyte-specific vascular expression of SARS-CoV-2 receptor ACE2 - implications for microvascular inflammation and hypercoagulopathy in COVID-19. Pathology 2020; 2020: 088500.
[http://dx.doi.org/10.1101/2020.05.11.088500]
[44]
Xia H, Lazartigues E. Angiotensin-converting enzyme 2: Central regulator for cardiovascular function. Curr Hypertens Rep 2010; 12(3): 170-5.
[http://dx.doi.org/10.1007/s11906-010-0105-7] [PMID: 20424953]
[45]
Gowrisankar YV, Clark MA. Angiotensin II regulation of angiotensin-converting enzymes in spontaneously hypertensive rat primary astrocyte cultures. J Neurochem 2016; 138(1): 74-85.
[http://dx.doi.org/10.1111/jnc.13641] [PMID: 27085714]
[46]
Duvernoy HM, Risold P-Y. The circumventricular organs: An atlas of comparative anatomy and vascularization. Brain Res Brain Res Rev 2007; 56(1): 119-47.
[http://dx.doi.org/10.1016/j.brainresrev.2007.06.002] [PMID: 17659349]
[47]
Li K, Wohlford-Lenane C, Perlman S, et al. Middle east respiratory syndrome coronavirus causes multiple organ damage and lethal disease in mice transgenic for human dipeptidyl peptidase 4. J Infect Dis 2016; 213(5): 712-22.
[http://dx.doi.org/10.1093/infdis/jiv499] [PMID: 26486634]
[48]
Tremblay M-E, Madore C, Bordeleau M, Tian L, Verkhratsky A. Neuropathobiology of COVID-19: The Role for Glia. Front Cell Neurosci 2020; 14: 592214.
[http://dx.doi.org/10.3389/fncel.2020.592214] [PMID: 33304243]
[49]
Swanson PA II, McGavern DB. Viral diseases of the central nervous system. Curr Opin Virol 2015; 11: 44-54.
[http://dx.doi.org/10.1016/j.coviro.2014.12.009] [PMID: 25681709]
[50]
Desforges M, Le Coupanec A, Stodola JK, Meessen-Pinard M, Talbot PJ. Human coronaviruses: Viral and cellular factors involved in neuroinvasiveness and neuropathogenesis. Virus Res 2014; 194: 145-58.
[http://dx.doi.org/10.1016/j.virusres.2014.09.011] [PMID: 25281913]
[51]
Li Y-C, Bai W-Z, Hirano N, Hayashida T, Hashikawa T. Coronavirus infection of rat dorsal root ganglia: Ultrastructural characterization of viral replication, transfer, and the early response of satellite cells. Virus Res 2012; 163(2): 628-35.
[http://dx.doi.org/10.1016/j.virusres.2011.12.021] [PMID: 22248641]
[52]
Berth SH, Leopold PL, Morfini GN. Virus-induced neuronal dysfunction and degeneration. Front Biosci 2009; 14(14): 5239-59.
[http://dx.doi.org/10.2741/3595] [PMID: 19482613]
[53]
Glass WG, Subbarao K, Murphy B, Murphy PM. Mechanisms of host defense following severe acute respiratory syndrome-coronavirus (SARS-CoV) pulmonary infection of mice. J Immunol 2004; 173(6): 4030-9.
[http://dx.doi.org/10.4049/jimmunol.173.6.4030] [PMID: 15356152]
[54]
Panwar B, Menon R, Eksi R, Li H-D, Omenn GS, Guan Y. Genome-wide functional annotation of human protein-coding splice variants using multiple instance learning. J Proteome Res 2016; 15(6): 1747-53.
[http://dx.doi.org/10.1021/acs.jproteome.5b00883] [PMID: 27142340]
[55]
Guo Y, Korteweg C, McNutt MA, Gu J. Pathogenetic mechanisms of severe acute respiratory syndrome. Virus Res 2008; 133(1): 4-12.
[http://dx.doi.org/10.1016/j.virusres.2007.01.022] [PMID: 17825937]
[56]
Bergmann CC, Lane TE, Stohlman SA. Coronavirus infection of the central nervous system: Host-virus stand-off. Nat Rev Microbiol 2006; 4(2): 121-32.
[http://dx.doi.org/10.1038/nrmicro1343] [PMID: 16415928]
[57]
Wang W, Xu Y, Gao R, et al. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA 2020; 323: 1843-4.
[http://dx.doi.org/10.1001/jama.2020.3786]
[58]
Zheng S, Fan J, Yu F, et al. Viral load dynamics and disease severity in patients infected with SARS-CoV-2 in Zhejiang province, China, January-March 2020: Retrospective cohort study. BMJ 2020; 369: m1443.
[http://dx.doi.org/10.1136/bmj.m1443] [PMID: 32317267]
[59]
Erickson MA, Banks WA. Neuroimmune axes of the blood-brain barriers and blood-brain interfaces: Bases for physiological regulation, disease states, and pharmacological interventions. Pharmacol Rev 2018; 70(2): 278-314.
[http://dx.doi.org/10.1124/pr.117.014647] [PMID: 29496890]
[60]
Daniels BP, Holman DW, Cruz-Orengo L, Jujjavarapu H, Durrant DM, Klein RS. Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals. MBio 2014; 5(5): e01476-14.
[http://dx.doi.org/10.1128/mBio.01476-14] [PMID: 25161189]
[61]
Al-Dalahmah O, Thakur KT, Nordvig AS, et al. Neuronophagia and microglial nodules in a SARS-CoV-2 patient with cerebellar hemorrhage. Acta Neuropathol Commun 2020; 8(1): 147.
[http://dx.doi.org/10.1186/s40478-020-01024-2] [PMID: 32847628]
[62]
Talbot PJ, Jacomy H, Desforges M. Pathogenesis of human coronaviruses other than severe acute respiratory syndrome coronavirus Nidoviruses. Washington, DC, USA: ASM Press 2014; pp. 313-24.
[http://dx.doi.org/10.1128/9781555815790.ch20]
[63]
Dando SJ, Mackay-Sim A, Norton R, et al. Pathogens penetrating the central nervous system: Infection pathways and the cellular and molecular mechanisms of invasion. Clin Microbiol Rev 2014; 27(4): 691-726.
[http://dx.doi.org/10.1128/CMR.00118-13] [PMID: 25278572]
[64]
Alyu F, Dikmen M. Inflammatory aspects of epileptogenesis: Contribution of molecular inflammatory mechanisms. Acta Neuropsychiatr 2017; 29(1): 1-16.
[http://dx.doi.org/10.1017/neu.2016.47] [PMID: 27692004]
[65]
Samuelsson A-M, Jennische E, Hansson H-A, Holmäng A. Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning. Am J Physiol Regul Integr Comp Physiol 2006; 290(5): R1345-56.
[http://dx.doi.org/10.1152/ajpregu.00268.2005] [PMID: 16357100]
[66]
Rana A, Musto AE. The role of inflammation in the development of epilepsy. J Neuroinflammation 2018; 15(1): 144.
[http://dx.doi.org/10.1186/s12974-018-1192-7] [PMID: 29764485]
[67]
Baig AM, Khaleeq A, Ali U, Syeda H. Evidence of the COVID-19 virus targeting the CNS: Tissue distribution, host-virus interaction, and proposed neurotropic mechanisms. ACS Chem Neurosci 2020; 11(7): 995-8.
[http://dx.doi.org/10.1021/acschemneuro.0c00122] [PMID: 32167747]
[68]
Cooper KW, Brann DH, Farruggia MC, et al. COVID-19 and the chemical senses: Supporting players take center stage. Neuron 2020; 107(2): 219-33.
[http://dx.doi.org/10.1016/j.neuron.2020.06.032] [PMID: 32640192]
[69]
Kanberg N, Ashton NJ, Andersson L-M, et al. Neurochemical evidence of astrocytic and neuronal injury commonly found in COVID-19. Neurology 2020; 95(12): e1754-9.
[http://dx.doi.org/10.1212/WNL.0000000000010111] [PMID: 32546655]
[70]
Pilotto A, Padovani A. ENCOVID-BIO network. Reply to the letter “COVID-19-Associated Encephalopathy and Cytokine-Mediated Neuroinflammation”. Ann Neurol 2020; 88(4): 861-2.
[http://dx.doi.org/10.1002/ana.25856] [PMID: 32737995]
[71]
Politi LS, Salsano E, Grimaldi M. Magnetic resonance imaging alteration of the brain in a patient with coronavirus disease 2019 (COVID-19) and anosmia. JAMA Neurol 2020; 77(8): 1028-9.
[http://dx.doi.org/10.1001/jamaneurol.2020.2125] [PMID: 32469400]
[72]
Dubé M, Le Coupanec A, Wong AHM, Rini JM, Desforges M, Talbot PJ. Axonal transport enables neuron-to-neuron propagation of human coronavirus OC43. J Virol 2018; 92(17): e00404-18.
[http://dx.doi.org/10.1128/JVI.00404-18] [PMID: 29925652]
[73]
Gautier J-F, Ravussin Y. A New Symptom of COVID-19: Loss of Taste and Smell. Obesity (Silver Spring) 2020; 28(5): 848.
[http://dx.doi.org/10.1002/oby.22809] [PMID: 32237199]
[74]
Giacomelli A, Pezzati L, Conti F, et al. Self-reported olfactory and taste disorders in patients with severe acute respiratory coronavirus 2 infection: A cross-sectional study. Clin Infect Dis 2020; 71(15): 889-90.
[http://dx.doi.org/10.1093/cid/ciaa330] [PMID: 32215618]
[75]
Lechien JR, Chiesa-Estomba CM, De Siati DR, et al. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): A multicenter European study. Eur Arch Otorhinolaryngol 2020; 277(8): 2251-61.
[http://dx.doi.org/10.1007/s00405-020-05965-1] [PMID: 32253535]
[76]
Lima M, Siokas V, Aloizou A-M, et al. Unraveling the possible routes of SARS-COV-2 invasion into the central nervous system. Curr Treat Options Neurol 2020; 22(11): 37.
[http://dx.doi.org/10.1007/s11940-020-00647-z] [PMID: 32994698]
[77]
Pennisi M, Lanza G, Falzone L, Fisicaro F, Ferri R, Bella R. SARS-CoV-2 and the nervous system: From clinical features to molecular mechanisms. Int J Mol Sci 2020; 21(15): E5475.
[http://dx.doi.org/10.3390/ijms21155475] [PMID: 32751841]
[78]
Iadecola C, Anrather J, Kamel H. Effects of COVID-19 on the Nervous System. Cell 2020; 183: 16-27.
[http://dx.doi.org/10.1016/j.cell.2020.08.028]
[79]
Desforges M, Le Coupanec A, Brison E, Meessen-Pinard M, Talbot PJ. Neuroinvasive and neurotropic human respiratory coronaviruses: Potential neurovirulent agents in humans. Adv Exp Med Biol 2014; 807: 75-96.
[http://dx.doi.org/10.1007/978-81-322-1777-0_6] [PMID: 24619619]
[80]
Zubair AS, McAlpine LS, Gardin T, Farhadian S, Kuruvilla DE, Spudich S. Neuropathogenesis and neurologic manifestations of the coronaviruses in the age of coronavirus disease 2019: A review. JAMA Neurol 2020; 77(8): 1018-27.
[http://dx.doi.org/10.1001/jamaneurol.2020.2065] [PMID: 32469387]
[81]
Kim W-K, Corey S, Alvarez X, Williams K. Monocyte/macrophage traffic in HIV and SIV encephalitis. J Leukoc Biol 2003; 74(5): 650-6.
[http://dx.doi.org/10.1189/jlb.0503207] [PMID: 12960230]
[82]
Dey J, Alam MT, Chandra S, et al. Neuroinvasion of SARS-CoV-2 may play a role in the breakdown of the respiratory center of the brain. J Med Virol 2021; 93(3): 1296-303.
[http://dx.doi.org/10.1002/jmv.26521] [PMID: 32964419]
[83]
Paniz-Mondolfi A, Bryce C, Grimes Z, et al. Central nervous system involvement by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). J Med Virol 2020; 92(7): 699-702.
[http://dx.doi.org/10.1002/jmv.25915] [PMID: 32314810]
[84]
Tseng C-TK, Huang C, Newman P, et al. Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human Angiotensin-converting enzyme 2 virus receptor. J Virol 2007; 81(3): 1162-73.
[http://dx.doi.org/10.1128/JVI.01702-06] [PMID: 17108019]
[85]
Roman M, Irwin MR. Novel neuroimmunologic therapeutics in depression: A clinical perspective on what we know so far. Brain Behav Immun 2020; 83: 7-21.
[http://dx.doi.org/10.1016/j.bbi.2019.09.016] [PMID: 31550500]
[86]
Chen Z, John Wherry E. T cell responses in patients with COVID-19. Nat Rev Immunol 2020; 20(9): 529-36.
[http://dx.doi.org/10.1038/s41577-020-0402-6] [PMID: 32728222]
[87]
Beigel JH, Farrar J, Han AM, et al. Avian influenza A (H5N1) infection in humans. N Engl J Med 2005; 353(13): 1374-85.
[http://dx.doi.org/10.1056/NEJMra052211] [PMID: 16192482]
[88]
Liddelow SA, Guttenplan KA, Clarke LE, et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 2017; 541(7638): 481-7.
[http://dx.doi.org/10.1038/nature21029] [PMID: 28099414]
[89]
Vasek MJ, Garber C, Dorsey D, et al. A complement-microglial axis drives synapse loss during virus-induced memory impairment. Nature 2016; 534(7608): 538-43.
[http://dx.doi.org/10.1038/nature18283] [PMID: 27337340]
[90]
Kooistra EJ, Waalders NJB, Grondman I, et al. RCI-COVID-19 Study Group. Anakinra treatment in critically ill COVID-19 patients: A prospective cohort study. Crit Care 2020; 24(1): 688.
[http://dx.doi.org/10.1186/s13054-020-03364-w] [PMID: 33302991]
[91]
Kyriazopoulou E, Poulakou G, Milionis H, et al. Early treatment of COVID-19 with anakinra guided by soluble urokinase plasminogen receptor plasma levels: A double-blind, randomized controlled phase 3 trial. Nat Med 2021; 27(10): 1752-60.
[http://dx.doi.org/10.1038/s41591-021-01499-z] [PMID: 34480127]
[92]
Kaplon H, Reichert JM. Antibodies to watch in 2018. MAbs 2018; 10(2): 183-203.
[http://dx.doi.org/10.1080/19420862.2018.1415671] [PMID: 29300693]
[93]
Zuber B, Rudström K, Ehrnfelt C, Ahlborg N. Epitope mapping of neutralizing monoclonal antibodies to human interferon-γ using human-bovine interferon-γ chimeras. J Interferon Cytokine Res 2016; 36(9): 542-51.
[http://dx.doi.org/10.1089/jir.2016.0017] [PMID: 27336613]
[94]
Stallmach A, Kortgen A, Gonnert F, Coldewey SM, Reuken P, Bauer M. Infliximab against severe COVID-19-induced cytokine storm syndrome with organ failure-a cautionary case series. Crit Care 2020; 24(1): 444.
[http://dx.doi.org/10.1186/s13054-020-03158-0] [PMID: 32680535]
[95]
Gritti G, Raimondi F, Bottazzi B, et al. Siltuximab downregulates interleukin-8 and pentraxin 3 to improve ventilatory status and survival in severe COVID-19. Leukemia 2021; 35(9): 2710-4.
[http://dx.doi.org/10.1038/s41375-021-01299-x] [PMID: 34031531]
[96]
Tanaka T, Narazaki M, Kishimoto T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol 2014; 6(10): a016295.
[http://dx.doi.org/10.1101/cshperspect.a016295] [PMID: 25190079]
[97]
Moore EE, Moore FA, Harken AH, Johnson JL, Ciesla D, Banerjee A. The two-event construct of postinjury multiple organ failure. Shock 2005; 24 (Suppl. 1): 71-4.
[http://dx.doi.org/10.1097/01.shk.0000191336.01036.fe] [PMID: 16374376]
[98]
Steinberg BE, Sundman E, Terrando N, Eriksson LI, Olofsson PS. Neural control of inflammation: Implications for perioperative and critical care. Anesthesiology 2016; 124(5): 1174-89.
[http://dx.doi.org/10.1097/ALN.0000000000001083] [PMID: 26982508]
[99]
Pavlov VA, Tracey KJ. Neural regulation of immunity: Molecular mechanisms and clinical translation. Nat Neurosci 2017; 20(2): 156-66.
[http://dx.doi.org/10.1038/nn.4477] [PMID: 28092663]
[100]
Tufan A, Avanoğlu Güler A, Matucci-Cerinic M. COVID-19, immune system response, hyperinflammation and repurposing antirheumatic drugs. Turk J Med Sci 2020; 50(SI-1): 620-32.
[http://dx.doi.org/10.3906/sag-2004-168] [PMID: 32299202]
[101]
Pavlov VA, Tracey KJ. The cholinergic anti-inflammatory pathway. Brain Behav Immun 2005; 19(6): 493-9.
[http://dx.doi.org/10.1016/j.bbi.2005.03.015] [PMID: 15922555]
[102]
Tracey KJ. The inflammatory reflex. Nature 2002; 420(6917): 853-9.
[http://dx.doi.org/10.1038/nature01321] [PMID: 12490958]
[103]
Das G, Mukherjee N, Ghosh S. Neurological insights of COVID-19 pandemic. ACS Chem Neurosci 2020; 11(9): 1206-9.
[http://dx.doi.org/10.1021/acschemneuro.0c00201] [PMID: 32320211]
[104]
Brown EN, Lydic R, Schiff ND. General anesthesia, sleep, and coma. N Engl J Med 2010; 363(27): 2638-50.
[http://dx.doi.org/10.1056/NEJMra0808281] [PMID: 21190458]
[105]
Brown EN, Pavone KJ, Naranjo M. Multimodal general anesthesia: Theory and practice. Anesth Analg 2018; 127(5): 1246-58.
[http://dx.doi.org/10.1213/ANE.0000000000003668] [PMID: 30252709]
[106]
Pavlov VA, Wang H, Czura CJ, Friedman SG, Tracey KJ. The cholinergic anti-inflammatory pathway: A missing link in neuroimmunomodulation. Mol Med 2003; 9(5-8): 125-34.
[http://dx.doi.org/10.1007/BF03402177] [PMID: 14571320]
[107]
Baptista AF, Baltar A, Okano AH, et al. Applications of non-invasive neuromodulation for the management of disorders related to COVID-19. Front Neurol 2020; 11: 573718.
[http://dx.doi.org/10.3389/fneur.2020.573718] [PMID: 33324324]
[108]
Huston JM. The vagus nerve and the inflammatory reflex: Wandering on a new treatment paradigm for systemic inflammation and sepsis. Surg Infect (Larchmt) 2012; 13(4): 187-93.
[http://dx.doi.org/10.1089/sur.2012.126] [PMID: 22913335]
[109]
Farsalinos K, Niaura R, Le Houezec J, et al. Editorial: Nicotine and SARS-CoV-2: COVID-19 may be a disease of the nicotinic cholinergic system. Toxicol Rep 2020; 7: 658-63.
[http://dx.doi.org/10.1016/j.toxrep.2020.04.012] [PMID: 32355638]
[110]
Aragón-Benedí C, Oliver-Forniés P, Galluccio F, et al. Is the heart rate variability monitoring using the analgesia nociception index a predictor of illness severity and mortality in critically ill patients with COVID-19? A pilot study. PLoS One 2021; 16(3): e0249128.
[http://dx.doi.org/10.1371/journal.pone.0249128] [PMID: 33760875]
[111]
Helms J, Kremer S, Merdji H, et al. Neurologic features in severe SARS-CoV-2 infection. N Engl J Med 2020; 382(23): 2268-70.
[http://dx.doi.org/10.1056/NEJMc2008597] [PMID: 32294339]
[112]
Venkatesan A, Tunkel AR, Bloch KC, et al. International Encephalitis Consortium. Case definitions, diagnostic algorithms, and priorities in encephalitis: Consensus statement of the international encephalitis consortium. Clin Infect Dis 2013; 57(8): 1114-28.
[http://dx.doi.org/10.1093/cid/cit458] [PMID: 23861361]
[113]
Cipriani G, Danti S, Nuti A, Carlesi C, Lucetti C, Di Fiorino M. A complication of coronavirus disease 2019: Delirium. Acta Neurol Belg 2020; 120(4): 927-32.
[http://dx.doi.org/10.1007/s13760-020-01401-7] [PMID: 32524537]
[114]
Pezzini A, Padovani A. Lifting the mask on neurological manifestations of COVID-19. Nat Rev Neurol 2020; 16(11): 636-44.
[http://dx.doi.org/10.1038/s41582-020-0398-3] [PMID: 32839585]
[115]
Scoppettuolo P, Borrelli S, Naeije G. Neurological involvement in SARS-CoV-2 infection: A clinical systematic review. Health 2020; 5: 100094.
[http://dx.doi.org/10.1016/j.bbih.2020.100094] [PMID: 33521692]
[116]
Kihira S, Delman BN, Belani P, et al. Imaging features of acute encephalopathy in patients with COVID-19: A case series. AJNR Am J Neuroradiol 2020; 41(10): 1804-8.
[http://dx.doi.org/10.3174/ajnr.A6715] [PMID: 32816764]
[117]
Luigetti M, Iorio R, Bentivoglio AR, et al. Gemelli against COVID-19 group. Assessment of neurological manifestations in hospitalized patients with COVID-19. Eur J Neurol 2020; 27(11): 2322-8.
[http://dx.doi.org/10.1111/ene.14444] [PMID: 32681611]
[118]
Paterson RW, Brown RL, Benjamin L, et al. The emerging spectrum of COVID-19 neurology: Clinical, radiological and laboratory findings. Brain 2020; 143(10): 3104-20.
[http://dx.doi.org/10.1093/brain/awaa240] [PMID: 32637987]
[119]
Ghosh R, Dubey S, Finsterer J, Chatterjee S, Ray BK. SARS-CoV-2-Associated acute hemorrhagic, necrotizing encephalitis (AHNE) presenting with cognitive impairment in a 44-year-old woman without comorbidities: A case report. Am J Case Rep 2020; 21: e925641.
[http://dx.doi.org/10.12659/AJCR.925641] [PMID: 32799213]
[120]
Unnithan AKA. A brief review of the neurological manifestations of the coronavirus disease. Egypt J Neurol Psychiat Neurosurg 2020; 56(1): 109.
[http://dx.doi.org/10.1186/s41983-020-00244-6] [PMID: 33250631]
[121]
Dogan L, Kaya D, Sarikaya T, et al. Plasmapheresis treatment in COVID-19-related autoimmune meningoencephalitis: Case series. Brain Behav Immun 2020; 87: 155-8.
[http://dx.doi.org/10.1016/j.bbi.2020.05.022] [PMID: 32389697]
[122]
Cao A, Rohaut B, Le Guennec L, et al. CoCo-Neurosciences study group. Severe COVID-19-related encephalitis can respond to immunotherapy. Brain 2020; 143(12): e102.
[http://dx.doi.org/10.1093/brain/awaa337] [PMID: 33064794]
[123]
Radmard S, Epstein SE, Roeder HJ, et al. Inpatient neurology consultations during the onset of the SARS-CoV-2 New York city pandemic: A single center case series. Front Neurol 2020; 11: 805.
[http://dx.doi.org/10.3389/fneur.2020.00805] [PMID: 32754113]
[124]
Siow I, Lee KS, Zhang JJY, Saffari SE, Ng A. Encephalitis as a neurological complication of COVID-19: A systematic review and meta-analysis of incidence, outcomes, and predictors. Eur J Neurol 2021; 28(10): 3491-502.
[http://dx.doi.org/10.1111/ene.14913] [PMID: 33982853]
[125]
McGill F, Griffiths MJ, Solomon T. Viral meningitis: Current issues in diagnosis and treatment. Curr Opin Infect Dis 2017; 30(2): 248-56.
[http://dx.doi.org/10.1097/QCO.0000000000000355] [PMID: 28118219]
[126]
Wright WF, Pinto CN, Palisoc K, Baghli S. Viral (aseptic) meningitis: A review. J Neurol Sci 2019; 398: 176-83.
[http://dx.doi.org/10.1016/j.jns.2019.01.050] [PMID: 30731305]
[127]
Sadarangani M, Willis L, Kadambari S, et al. Childhood meningitis in the conjugate vaccine era: A prospective cohort study. Arch Dis Child 2015; 100(3): 292-4.
[http://dx.doi.org/10.1136/archdischild-2014-306813] [PMID: 25256088]
[128]
Mijovic H, Sadarangani M. To LP or not to LP? Identifying the etiology of pediatric meningitis. Pediatr Infect Dis J 2019; 38(6S) (Suppl. 1): S39-42.
[http://dx.doi.org/10.1097/INF.0000000000002313] [PMID: 31205243]
[129]
Logan SAE, MacMahon E. Viral meningitis. BMJ 2008; 336(7634): 36-40.
[http://dx.doi.org/10.1136/bmj.39409.673657.AE] [PMID: 18174598]
[130]
Negrini B, Kelleher KJ, Wald ER. Cerebrospinal fluid findings in aseptic versus bacterial meningitis. Pediatrics 2000; 105(2): 316-9.
[http://dx.doi.org/10.1542/peds.105.2.316] [PMID: 10654948]
[131]
Fiest KM, Sauro KM, Wiebe S, et al. Prevalence and incidence of epilepsy: A systematic review and meta-analysis of international studies. Neurology 2017; 88(3): 296-303.
[http://dx.doi.org/10.1212/WNL.0000000000003509] [PMID: 27986877]
[132]
Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in china: Summary of a report of 72 314 cases from the Chinese center for disease control and prevention. JAMA 2020; 323(13): 1239-42.
[http://dx.doi.org/10.1001/jama.2020.2648] [PMID: 32091533]
[133]
Jordan RE, Adab P, Cheng KK. Covid-19: Risk factors for severe disease and death. BMJ 2020; 368: m1198.
[http://dx.doi.org/10.1136/bmj.m1198] [PMID: 32217618]
[134]
Lu Q, Shi Y. Coronavirus disease (COVID-19) and neonate: What neonatologist need to know. J Med Virol 2020; 92(6): 564-7.
[http://dx.doi.org/10.1002/jmv.25740] [PMID: 32115733]
[135]
De Sanctis P, Doneddu PE, Viganò L, Selmi C, Nobile-Orazio E. Guillain-Barré syndrome associated with SARS-CoV-2 infection. A systematic review. Eur J Neurol 2020; 27(11): 2361-70.
[http://dx.doi.org/10.1111/ene.14462] [PMID: 32757404]
[136]
Filosto M, Cotti Piccinelli S, Gazzina S, et al. Guillain-Barré syndrome and COVID-19: An observational multicentre study from two Italian hotspot regions. J Neurol Neurosurg Psychiatry 2021; 92(7): 751-6.
[http://dx.doi.org/10.1136/jnnp-2020-324837] [PMID: 33158914]
[137]
Hasan I, Saif-Ur-Rahman KM, Hayat S, et al. Guillain-Barré syndrome associated with SARS-CoV-2 infection: A systematic review and individual participant data meta-analysis. J Peripher Nerv Syst 2020; 25(4): 335-43.
[http://dx.doi.org/10.1111/jns.12419] [PMID: 33112450]
[138]
Luijten LWG, Leonhard SE, van der Eijk AA, et al. IGOS consortium. Guillain-Barré syndrome after SARS-CoV-2 infection in an international prospective cohort study. Brain J Neurol 2021; 2021: awab279.
[http://dx.doi.org/10.1093/brain/awab279]
[139]
Cornblath DR. Electrophysiology in Guillain-Barré syndrome. Ann Neurol 1990; 27 (Suppl. 1): S17-20.
[http://dx.doi.org/10.1002/ana.410270706] [PMID: 2194420]
[140]
Shorr AF, Thomas SJ, Alkins SA, Fitzpatrick TM, Ling GS. D-dimer correlates with proinflammatory cytokine levels and outcomes in critically ill patients. Chest 2002; 121(4): 1262-8.
[http://dx.doi.org/10.1378/chest.121.4.1262] [PMID: 11948062]
[141]
Parra B, Lizarazo J, Jiménez-Arango JA, et al. Guillain-barré syndrome associated with zika virus infection in Colombia. N Engl J Med 2016; 375(16): 1513-23.
[http://dx.doi.org/10.1056/NEJMoa1605564] [PMID: 27705091]
[142]
Toscano G, Palmerini F, Ravaglia S, et al. Guillain-barré syndrome associated with SARS-CoV-2. N Engl J Med 2020; 382(26): 2574-6.
[http://dx.doi.org/10.1056/NEJMc2009191] [PMID: 32302082]
[143]
Transverse myelitis fact sheet | National Institute of neurological disorders and stroke. Available from: https://www.ninds.nih.gov/Disorders/Patient-Caregiver-Education/Fact-Sheets/Transverse-Myelitis-Fact-Sheet (Accessed on: September 30, 2021).
[144]
Transverse Myelitis Consortium Working Group. Proposed diagnostic criteria and nosology of acute transverse myelitis. Neurology 2002; 59(4): 499-505.
[http://dx.doi.org/10.1212/WNL.59.4.499] [PMID: 12236201]
[145]
Beh SC, Greenberg BM, Frohman T, Frohman EM. Transverse myelitis. Neurol Clin 2013; 31(1): 79-138.
[http://dx.doi.org/10.1016/j.ncl.2012.09.008] [PMID: 23186897]
[146]
Borchers AT, Gershwin ME. Transverse myelitis. Autoimmun Rev 2012; 11(3): 231-48.
[http://dx.doi.org/10.1016/j.autrev.2011.05.018] [PMID: 21621005]
[147]
Winkelmann A, Loebermann M, Reisinger EC, Hartung H-P, Zettl UK. Disease-modifying therapies and infectious risks in multiple sclerosis. Nat Rev Neurol 2016; 12(4): 217-33.
[http://dx.doi.org/10.1038/nrneurol.2016.21] [PMID: 26943779]
[148]
Adamczyk-Sowa M, Mado H, Kubicka-Bączyk K, et al. SARS-CoV-2/COVID-19 in multiple sclerosis patients receiving disease-modifying therapy. Clin Neurol Neurosurg 2021; 201: 106451.
[http://dx.doi.org/10.1016/j.clineuro.2020.106451] [PMID: 33388661]
[149]
Louapre C, Collongues N, Stankoff B, et al. Covisep investigators. Clinical characteristics and outcomes in patients with coronavirus disease 2019 and multiple sclerosis. JAMA Neurol 2020; 77(9): 1079-88.
[http://dx.doi.org/10.1001/jamaneurol.2020.2581] [PMID: 32589189]
[150]
Lublin FD, Reingold SC, Cohen JA, et al. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology 2014; 83(3): 278-86.
[http://dx.doi.org/10.1212/WNL.0000000000000560] [PMID: 24871874]
[151]
Parrotta E, Kister I, Charvet L, et al. COVID-19 outcomes in MS: Observational study of early experience from NYU Multiple Sclerosis Comprehensive Care Center. Neurol Neuroimmunol Neuroinflamm 2020; 7(5): e835.
[http://dx.doi.org/10.1212/NXI.0000000000000835] [PMID: 32646885]
[152]
Brownlee W, Bourdette D, Broadley S, Killestein J, Ciccarelli O. Treating multiple sclerosis and neuromyelitis optica spectrum disorder during the COVID-19 pandemic. Neurology 2020; 94(22): 949-52.
[http://dx.doi.org/10.1212/WNL.0000000000009507] [PMID: 32241953]
[153]
De Angelis M, Petracca M, Lanzillo R, Brescia Morra V, Moccia M. Mild or no COVID-19 symptoms in cladribine-treated multiple sclerosis: Two cases and implications for clinical practice. Mult Scler Relat Disord 2020; 45: 102452.
[http://dx.doi.org/10.1016/j.msard.2020.102452] [PMID: 32823148]
[154]
Leist TP, Weissert R. Cladribine: Mode of action and implications for treatment of multiple sclerosis. Clin Neuropharmacol 2011; 34(1): 28-35.
[http://dx.doi.org/10.1097/WNF.0b013e318204cd90] [PMID: 21242742]
[155]
Havrdova E, Horakova D, Kovarova I. Alemtuzumab in the treatment of multiple sclerosis: Key clinical trial results and considerations for use. Ther Adv Neurol Disord 2015; 8(1): 31-45.
[http://dx.doi.org/10.1177/1756285614563522] [PMID: 25584072]
[156]
Hu Y, Turner MJ, Shields J, et al. Investigation of the mechanism of action of alemtuzumab in a human CD52 transgenic mouse model. Immunology 2009; 128(2): 260-70.
[http://dx.doi.org/10.1111/j.1365-2567.2009.03115.x] [PMID: 19740383]
[157]
Mulero P, Midaglia L, Montalban X. Ocrelizumab: A new milestone in multiple sclerosis therapy. Ther Adv Neurol Disord 2018; 11: 1756286418773025.
[http://dx.doi.org/10.1177/1756286418773025] [PMID: 29774057]
[158]
Mease PJ. B cell-targeted therapy in autoimmune disease: Rationale, mechanisms, and clinical application. J Rheumatol 2008; 35(7): 1245-55.
[PMID: 18609733]
[159]
Chisari CG, Sgarlata E, Arena S, Toscano S, Luca M, Patti F. Rituximab for the treatment of multiple sclerosis: A review. J Neurol 2021.
[http://dx.doi.org/10.1007/s00415-020-10362-z] [PMID: 33416999]
[160]
Klein C, Lammens A, Schäfer W, et al. Epitope interactions of monoclonal antibodies targeting CD20 and their relationship to functional properties. MAbs 2013; 5(1): 22-33.
[http://dx.doi.org/10.4161/mabs.22771] [PMID: 23211638]
[161]
Chun J, Hartung H-P. Mechanism of action of oral fingolimod (FTY720) in multiple sclerosis. Clin Neuropharmacol 2010; 33(2): 91-101.
[http://dx.doi.org/10.1097/WNF.0b013e3181cbf825] [PMID: 20061941]
[162]
Behrangi N, Fischbach F, Kipp M. Mechanism of siponimod: Anti-inflammatory and neuroprotective mode of action. Cells 2019; 8(1): E24.
[http://dx.doi.org/10.3390/cells8010024] [PMID: 30621015]
[163]
Lassiter G, Melancon C, Rooney T, et al. Ozanimod to treat relapsing forms of multiple sclerosis: A comprehensive review of disease, drug efficacy and side effects. Neurol Int 2020; 12(3): 89-108.
[http://dx.doi.org/10.3390/neurolint12030016] [PMID: 33287177]
[164]
Léger OJ, Yednock TA, Tanner L, et al. Humanization of a mouse antibody against human alpha-4 integrin: A potential therapeutic for the treatment of multiple sclerosis. Hum Antibodies 1997; 8(1): 3-16.
[http://dx.doi.org/10.3233/HAB-1997-8102] [PMID: 9265500]
[165]
Hutchinson M. Natalizumab: A new treatment for relapsing remitting multiple sclerosis. Ther Clin Risk Manag 2007; 3(2): 259-68.
[http://dx.doi.org/10.2147/tcrm.2007.3.2.259] [PMID: 18360634]
[166]
Linker RA, Lee D-H, Ryan S, et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain 2011; 134(Pt 3): 678-92.
[http://dx.doi.org/10.1093/brain/awq386] [PMID: 21354971]
[167]
Bar-Or A, Pachner A, Menguy-Vacheron F, Kaplan J, Wiendl H. Teriflunomide and its mechanism of action in multiple sclerosis. Drugs 2014; 74(6): 659-74.
[http://dx.doi.org/10.1007/s40265-014-0212-x] [PMID: 24740824]
[168]
Ziemssen T, Schrempf W. Glatiramer acetate: Mechanisms of action in multiple sclerosis. Int Rev Neurobiol 2007; 79: 537-70.
[http://dx.doi.org/10.1016/S0074-7742(07)79024-4] [PMID: 17531858]
[169]
Kieseier BC. The mechanism of action of interferon-β in relapsing multiple sclerosis. CNS Drugs 2011; 25(6): 491-502.
[http://dx.doi.org/10.2165/11591110-000000000-00000] [PMID: 21649449]

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