AccScience Publishing / AN / Online First / DOI: 10.36922/an.1319
Submit to AN
Cite this article
154
Download
2363
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
REVIEW

Multiple sclerosis: Unveiling current immunogenetic factors and their role in etiopathogenesis and clinical aspects

Benediktas Trumpulis1* ,  Rasa Liutkeviciene2 ,  Renata Balnyte3
Show Less
1 Lithuanian University of Health Sciences, Medical Academy, Eiveniu 2 Street, Kaunas, Lithuania
2 Neuroscience Instituten University of Health Sciences, Medical Academy, Eiveniu Street 2, Kaunas, Lithuania
3 Department of Neurologyn University of Health Sciences, Medical Academy, Eiveniu 2 Street, Kaunas, Lithuania
Advanced Neurology 2023, 2(3), 1319 https://doi.org/10.36922/an.1319
Submitted: 18 July 2023 | Accepted: 14 September 2023 | Published: 29 September 2023
© 2023 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Download PDF
Cite
XML
Abstract

Multiple sclerosis (MS) is the most common cause of neurological deficits among the young population. While the prevalence of MS is increasing worldwide, the incidence rate of MS is also undergoing a similar trend in Lithuania. Globally, women are twice as likely to be affected by MS as men. Unilateral optic neuritis is the most common initial symptom of MS. The signs and symptoms of MS vary greatly from patient to patient and depend on the location and severity of the nerve fiber damage in the central nervous system. Most people with MS have a relapsing-remitting disease course or clinically isolated syndrome. They experience periods of new symptoms or relapses that develop over days or weeks and usually resolve partially or completely. These relapses are followed by quiet periods of disease remission that may last months or even years. Data accumulated over the years suggest a complex interplay between environment and immunogenetics (strong associations with a large number of immune and genetic markers), and an increasingly convincing role of an underlying degenerative process leading to demyelination (in both white and gray matter), axonal and neurosynaptic damage, and a persistent innate inflammatory response, with T-cell-mediated autoimmunity appearing to play a diminishing role as the MS develops and progresses. In the absence of clinically proven, accurate, and reliable biomarkers, the disease can take a progressive course in case of late treatment, signifying the critical need for early diagnosis. This article therefore discusses the etiopathogenesis and clinical aspects of MS.

Keywords
Multiple sclerosis
Etiopathogenesis
Clinical aspects
Funding
None.
Conflict of interest
The authors declare they have no competing interests.
References
  1. Wallin MT, Culpepper WJ, Nichols E, et al., 2019, Global, regional, and national burden of multiple sclerosis 1990– 2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol, 18: 269–285. https://doi.org/10.1016/S1474-4422(18)30443-5

 

  1. Walton C, King R, Rechtman L, et al., 2020, Rising prevalence of multiple sclerosis worldwide: Insights from the Atlas of MS, third edition. Mult Scler, 26: 1816–1821. https://doi.org/10.1177/1352458520970841

 

  1. Leray E, Moreau T, Fromont A, et al., 2016, Epidemiology of multiple sclerosis. Rev Neurol (Paris), 172: 3–13. https://doi.org/10.1016/j.neurol.2015.10.006

 

  1. Valadkeviciene D, Kavaliunas A, Kizlaitiene R, et al., 2019, Incidence rate and sex ratio in multiple sclerosis in Lithuania. Brain Behav, 9: e01150. https://doi.org/10.1002/brb3.1150

 

  1. Yong HYF, Yong VW, 2022, Mechanism-based criteria to improve therapeutic outcomes in progressive multiple sclerosis. Nat Rev Neurol, 18: 40–55. https://doi.org/10.1038/s41582-021-00581-x

 

  1. Amezcua L, 2022, Progressive multiple sclerosis. Continuum (Minneap Minn), 28: 1083–1103. https://doi.org/10.1212/CON.0000000000001157

 

  1. Reich DS, Lucchinetti CF, Calabresi PA, 2018, Multiple sclerosis. N Engl J Med, 378: 169–180. https://doi.org/10.1056/NEJMra1401483

 

  1. Stys PK, Tsutsui S, 2019, Recent advances in understanding multiple sclerosis. F1000Res, 8: 2100. https://doi.org/10.12688/f1000research.20906.1

 

  1. Sellebjerg F, Börnsen L, Ammitzbøll C, et al., 2017, Defining active progressive multiple sclerosis. Mult Scler, 23: 1727–1735. https://doi.org/10.1177/1352458517726592

 

  1. Pozzilli C, Pugliatti M, Vermersch P, et al., 2023, Diagnosis and treatment of progressive multiple sclerosis: A position paper. Eur J Neurol, 30: 9–21. https://doi.org/10.1111/ene.15593

 

  1. Ziemssen T, Bhan V, Chataway J, et al., 2023, Secondary progressive multiple sclerosis: A review of clinical characteristics, definition, prognostic tools, and disease-modifying therapies. Neurol Neuroimmunol Neuroinflamm, 10: e200064. https://doi.org/10.1212/NXI.0000000000200064

 

  1. Thompson AJ, Banwell BL, Barkhof F, et al., 2018, Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol, 17: 162–173. https://doi.org/10.1016/S1474-4422(17)30470-2

 

  1. Goodin DS, Khankhanian P, Gourraud PA, et al., 2021, The nature of genetic and environmental susceptibility to multiple sclerosis. PLoS One, 16: e0246157. https://doi.org/10.1371/journal.pone.0246157

 

  1. Gerdes LA, Janoschka C, Eveslage M, et al., 2020, Immune signatures of prodromal multiple sclerosis in monozygotic twins. Proc Natl Acad Sci U S A, 117: 21546–21556. https://doi.org/10.1073/pnas.2003339117

 

  1. Ortega-Hernandez OD, Martínez-Cáceres EM, Presas- Rodríguez S, et al., 2023, Epstein-barr virus and multiple sclerosis: A convoluted interaction and the opportunity to unravel predictive biomarkers. Int J Mol Sci, 24: 7407. https://doi.org/10.3390/ijms24087407

 

  1. Bjornevik K, Cortese M, Healy BC, et al., 2022, Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis. Science, 375: 296–301. https://doi.org/10.1126/science.abj8222

 

  1. Kuchroo VK, Weiner HL, 2022, How does Epstein-Barr virus trigger MS? Immunity, 55: 390–392. https://doi.org/10.1016/j.immuni.2022.02.008

 

  1. Vasileiou ES, Hu C, Bernstein CN, et al., 2022, Association of Vitamin D polygenic risk scores and disease outcome in people with multiple sclerosis. Neurol Neuroimmunol Neuroinflamm, 10: e20006. https://doi.org/10.1212/NXI.0000000000200062

 

  1. Watanabe M, Nakamura Y, Sato S, et al., 2021, HLA genotype-clinical phenotype correlations in multiple sclerosis and neuromyelitis optica spectrum disorders based on Japan MS/NMOSD Biobank data. Sci Rep, 11: 607. https://doi.org/10.1038/s41598-020-79833-7

 

  1. International Multiple Sclerosis Genetics Consortium, 2019, Multiple sclerosis genomic map implicates peripheral immune cells and microglia in susceptibility. Science, 365: eaav7188. https://doi.org/10.1126/science.aav7188

 

  1. Fitzgerald KC, Kim K, Smith MD, et al., 2019, Early complement genes are associated with visual system degeneration in multiple sclerosis. Brain, 142: 2722–2736. https://doi.org/10.1093/brain/awz188

 

  1. Gresle MM, Jordan MA, Stankovich J, et al., 2020, Multiple sclerosis risk variants regulate gene expression in innate and adaptive immune cells. Life Sci Alliance, 3: e202000650. https://doi.org/10.26508/lsa.202000650

 

  1. Baecher-Allan C, Kaskow BJ, Weiner HL, 2018, Multiple sclerosis: Mechanisms and immunotherapy. Neuron, 97: 742–768. https://doi.org/10.1016/j.neuron.2018.01.021

 

  1. Heidker RM, Emerson MR, LeVine SM, 2017, Metabolic pathways as possible therapeutic targets for progressive multiple sclerosis. Neural Regen Res, 12: 1262–1267. https://doi.org/10.4103/1673-5374.213542

 

  1. Lassmann H, 2018, Pathogenic mechanisms associated with different clinical courses of multiple sclerosis. Front Immunol, 9: 3116. https://doi.org/10.3389/fimmu.2018.03116

 

  1. Dong Y, Yong VW, 2019, When encephalitogenic T cells collaborate with microglia in multiple sclerosis. Nat Rev Neurol, 15: 704–717. https://doi.org/10.1038/s41582-019-0253-6

 

  1. Lisak RP, Nedelkoska L, Benjamins JA, et al., 2017, B cells from patients with multiple sclerosis induce cell death via apoptosis in neurons in vitro. J Neuroimmunol, 309: 88–99. https://doi.org/10.1016/j.jneuroim.2017.05.004

 

  1. Mahad DH, Trapp BD, Lassmann H, 2015, Pathological mechanisms in progressive multiple sclerosis. Lancet Neurol, 14: 183–193. https://doi.org/10.1016/S1474-4422(14)70256-X

 

  1. Sucksdorff M, Matilainen M, Tuisku J, et al., 2020, Brain TSPO-PET predicts later disease progression independent of relapses in multiple sclerosis. Brain, 143: 3318–3330. https://doi.org/10.1093/brain/awaa275

 

  1. Calabrese M, Magliozzi R, Ciccarelli O, et al., 2015, Exploring the origins of grey matter damage in multiple sclerosis. Nat Rev Neurosci, 16: 147–158. https://doi.org/10.1038/nrn3900

 

  1. Berghoff SA, Spieth L, Sun T, et al., 2021, Microglia facilitate repair of demyelinated lesions via post-squalene sterol synthesis. Nat Neurosci, 24: 47–60. https://doi.org/10.1038/s41593-020-00757-6

 

  1. Jäckle K, Zeis T, Schaeren-Wiemers N, et al., 2020, Molecular signature of slowly expanding lesions in progressive multiple sclerosis. Brain, 143: 2073–2088. https://doi.org/10.1093/brain/awaa158

 

  1. Campbell G, Mahad DJ, 2018, Mitochondrial dysfunction and axon degeneration in progressive multiple sclerosis. FEBS Lett, 592: 1113–1121. https://doi.org/10.1002/1873-3468.13013

 

  1. Licht-Mayer S, Campbell GR, Canizares M, et al., 2020, Enhanced axonal response of mitochondria to demyelination offers neuroprotection: Implications for multiple sclerosis. Acta Neuropathol, 140: 143–167. https://doi.org/10.1007/s00401-020-02179-x

 

  1. Campbell GR, Worrall JT, Mahad DJ, 2014, The central role of mitochondria in axonal degeneration in multiple sclerosis. Mult Scler, 20: 1806–1813. https://doi.org/10.1177/1352458514544537

 

  1. Abdelhak A, Hottenrott T, Mayer C, et al., 2017, CSF profile in primary progressive multiple sclerosis: Re-exploring the basics. PLoS One, 12: e0182647. https://doi.org/10.1371/journal.pone.0182647

 

  1. Lee NJ, Ha SK, Sati P, et al., 2019, Potential role of iron in repair of inflammatory demyelinating lesions. J Clin Invest, 129: 4365–4376. https://doi.org/10.1172/JCI126809

 

  1. Raz E, Branson B, Jensen JH, et al., 2015, Relationship between iron accumulation and white matter injury in multiple sclerosis: A case-control study. J Neurol, 262: 402–409. https://doi.org/10.1007/s00415-014-7569-3

 

  1. Lubetzki C, Zalc B, Williams A, et al., 2020, Remyelination in multiple sclerosis: From basic science to clinical translation. Lancet Neurol, 19: 678–688. https://doi.org/10.1016/S1474-4422(20)30140-X

 

  1. Micu I, Plemel JR, Caprariello AV, et al., 2018, Axo-myelinic neurotransmission: A novel mode of cell signalling in the central nervous system. Nat Rev Neurosci, 19: 49–58. https://doi.org/10.1038/nrn.2017.128

 

  1. Correale J, Gaitán MI, Ysrraelit MC, et al., 2017, Progressive multiple sclerosis: From pathogenic mechanisms to treatment. Brain, 140: 527–546. https://doi.org/10.1093/brain/aww258

 

  1. Bodini B, Veronese M, García-Lorenzo D, et al., 2016, Dynamic imaging of individual remyelination profiles in multiple sclerosis. Ann Neurol, 79: 726–738. https://doi.org/10.1002/ana.24620

 

  1. Franklin RJM, Frisén J, Lyons DA, 2021, Revisiting remyelination: Towards a consensus on the regeneration of CNS myelin. Semin Cell Dev Biol, 116: 3–9. https://doi.org/10.1016/j.semcdb.2020.09.009

 

  1. Schattling B, Engler JB, Volkmann C, et al., 2019, Bassoon proteinopathy drives neurodegeneration in multiple sclerosis. Nat Neurosci, 22: 887–896. https://doi.org/10.1038/s41593-019-0385-4

 

  1. Luchicchi A, Hart B, Frigerio I, et al., 2021, Axon-myelin unit blistering as early event in MS normal appearing white matter. Ann Neurol, 89: 711–725. https://doi.org/10.1002/ana.26014

 

  1. Schumacher AM, Mahler C, Kerschensteiner M, 2017, Pathology and pathogenesis of progressive multiple sclerosis: Concepts and controversies. Neurol Int Open, 1: E171–E181. https://doi.org/10.1055/s-0043-106704

 

  1. He A, Merkel B, Brown JWL, et al., 2020, Timing of high-efficacy therapy for multiple sclerosis: A retrospective observational cohort study. Lancet Neurol, 19: 307–316. https://doi.org/10.1016/S1474-4422(20)30067-3

 

  1. Tavazzi E, Zivadinov R, Dwyer MG, et al., 2020, MRI biomarkers of disease progression and conversion to secondary-progressive multiple sclerosis. Expert Rev Neurother, 20: 821–834. https://doi.org/10.1080/14737175.2020.1757435

 

  1. Filippi M, Preziosa P, Langdon D, et al., 2020, Identifying progression in multiple sclerosis: New perspectives. Ann Neurol, 88: 438–452. https://doi.org/10.1002/ana.25808

 

  1. Frischer JM, Weigand SD, Guo Y, et al., 2015, Clinical and pathological insights into the dynamic nature of the white matter multiple sclerosis plaque. Ann Neurol, 78: 710–721. https://doi.org/10.1002/ana.24497

 

  1. Absinta M, Sati P, Masuzzo F, et al., 2019, Association of chronic active multiple sclerosis lesions with disability in vivo. JAMA Neurol, 76: 1474–1483. https://doi.org/10.1001/jamaneurol.2019.2399

 

  1. Kaisey M, Lashgari G, Fert-Bober J, et al., 2022, An update on diagnostic laboratory biomarkers for multiple sclerosis. Curr Neurol Neurosci Rep, 22: 675–688. https://doi.org/10.1007/s11910-022-01227-1

 

  1. Williams T, Zetterberg H, Chataway J, 2021, Neurofilaments in progressive multiple sclerosis: A systematic review. J Neurol, 268: 3212–3222. https://doi.org/10.1007/s00415-020-09917-x

 

  1. Pitt D, Lo CH, Gauthier SA, et al., 2022, Toward precision phenotyping of multiple sclerosis. Neurol Neuroimmunol Neuroinflamm, 9: e200025. https://doi.org/10.1212/NXI.0000000000200025

 

  1. Siller N, Kuhle J, Muthuraman M, et al., 2019, Serum neurofilament light chain is a biomarker of acute and chronic neuronal damage in early multiple sclerosis. Mult Scler, 25: 678–686. https://doi.org/10.1177/1352458518765666

 

  1. Bjornevik K, Munger KL, Cortese M, et al., 2020, Serum neurofilament light chain levels in patients with presymptomatic multiple sclerosis. JAMA Neurol, 77: 58–64. https://doi.org/10.1001/jamaneurol.2019.3238

 

  1. Kapoor R, Smith KE, Allegretta M, et al., 2020, Serum neurofilament light as a biomarker in progressive multiple sclerosis. Neurology, 95: 436–444. https://doi.org/10.1212/WNL.0000000000010346

 

  1. Golabi M, Fathi F, Samadi M, et al., 2022, Identification of potential biomarkers in the peripheral blood mononuclear cells of relapsing-remitting multiple sclerosis patients. Inflammation, 45: 1815–1828. https://doi.org/10.1007/s10753-022-01662-9

 

  1. Abdelhak A, Huss A, Kassubek J, et al., 2018, Serum GFAP as a biomarker for disease severity in multiple sclerosis. Sci Rep, 8: 14798. https://doi.org/10.1038/s41598-018-33158-8

 

  1. Hou Y, Dan X, Babbar M, et al., 2019, Ageing as a risk factor for neurodegenerative disease. Nat Rev Neurol, 15: 565–581. https://doi.org/10.1038/s41582-019-0244-7

 

  1. Krysko KM, Henry RG, Cree BA, et al., 2019, Telomere length is associated with disability progression in multiple sclerosis. Ann Neurol, 86: 671–682. https://doi.org/10.1002/ana.25592

 

  1. Meca-Lallana V, Berenguer-Ruiz L, Carreres-Polo J, et al., 2021, Deciphering multiple sclerosis progression. Front Neurol, 12: 608491. https://doi.org/10.3389/fneur.2021.608491

 

  1. Sandelius Å, Sandgren S, Axelsson M, et al., 2019, Cerebrospinal fluid growth-associated protein 43 in multiple sclerosis. Sci Rep, 9: 17309. https://doi.org/10.1111/j.1365-2990.2006.00730.x

 

  1. Shah AA, Piche J, Stewart B, et al., 2023, Limited diagnostic utility of serologic testing for neurologic manifestations of systemic disease in the evaluation of suspected multiple sclerosis: A single-center observational study. Mult Scler Relat Disord, 69: 104443. https://doi.org/10.1016/j.msard.2022.104443

 

  1. Berer K, Gerdes LA, Cekanaviciute E, et al., 2017, Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc Natl Acad Sci U S A, 114: 10719–10724. https://doi.org/10.1073/pnas.1711233114

 

  1. Jangi S, Gandhi R, Cox LM, et al., 2016, Alterations of the human gut microbiome in multiple sclerosis. Nat Commun, 7: 12015. https://doi.org/10.1038/ncomms12015

 

  1. Cekanaviciute E, Yoo BB, Runia TF, et al., 2017, Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. Proc Natl Acad Sci U S A, 114: 10713–10718. https://doi.org/10.1073/pnas.1711235114

 

  1. Reynders T, Devolder L, Valles-Colomer M, et al., 2020, Gut microbiome variation is associated to multiple sclerosis phenotypic subtypes. Ann Clin Transl Neurol, 7: 406–419. https://doi.org/10.1002/acn3.51004

 

  1. Kappos L, Wolinsky JS, Giovannoni G, et al., 2020, Contribution of relapse-independent progression vs relapse-associated worsening to overall confirmed disability accumulation in typical relapsing multiple sclerosis in a pooled analysis of 2 randomized clinical trials. JAMA Neurol, 77: 1132–1140. https://doi.org/10.1001/jamaneurol.2020.1568

 

  1. Giovannoni G, Popescu V, Wuerfel J, et al., 2022, Smouldering multiple sclerosis: The “real MS”. Ther Adv Neurol Disord, 15: 17562864211066751. https://doi.orr/10.1177/17562864211066751

 

  1. Luchetti S, Fransen NL, Van Eden CG, et al., 2018, Progressive multiple sclerosis patients show substantial lesion activity that correlates with clinical disease severity and sex: A retrospective autopsy cohort analysis. Acta Neuropathol, 135: 511–528. https://doi.org/10.1007/s00401-018-1818-y

 

  1. Sastre-Garriga J, Pareto D, Rovira À, 2017, Brain atrophy in multiple sclerosis: Clinical relevance and technical aspects. Neuroimaging Clin N Am, 27: 289–300. https://doi.org/10.1016/j.nic.2017.01.002

 

  1. Tintore M, Vidal-Jordana A, Sastre-Garriga J, 2019, Treatment of multiple sclerosis-success from bench to bedside. Nat Rev Neurol, 15: 53–58. https://doi.org/10.1038/s41582-018-0082-z

 

  1. Koseoglu M, Tutuncu M, 2020, Conversion of optic neuritis to relapsing remitting multiple sclerosis: A retrospective comorbidity cohort study. Eur Neurol, 83: 287–292. https://doi.org/10.1159/000507547

 

  1. Abri Aghdam K, Aghajani A, Kanani F, et al., 2021, A novel decision tree approach to predict the probability of conversion to multiple sclerosis in Iranian patients with optic neuritis. Mult Scler Relat Disord, 47: 102658. https://doi.org/10.1016/j.msard.2020.102658

 

  1. Kenney R, Liu M, Patil S, et al., 2021, Long-term outcomes in patients presenting with optic neuritis: Analyses of the MSBase registry. J Neurol Sci, 430: 118067. https://doi.org/10.1016/j.jns.2021.118067

 

  1. Gu W, Tagg NT, Panchal NL, et al., 2021, Incidence of optic neuritis and the associated risk of multiple sclerosis for service members of U.S. Armed forces. Mil Med, 188: usab352. https://doi.org/10.1093/milmed/usab352

 

  1. Ysrraelit MC, Correale J, 2019, Impact of sex hormones on immune function and multiple sclerosis development. Immunology, 156: 9–22. https://doi.org/10.1111/imm.13004

 

  1. Lee JY, Han J, Yang M, et al., 2020, Population-based incidence of pediatric and adult optic neuritis and the risk of multiple sclerosis. Ophthalmology, 127: 417–425. https://doi.org/10.1016/j.ophtha.2019.09.032

 

  1. Pihl-Jensen G, Wanscher B, Frederiksen JL, 2021, Predictive value of optical coherence tomography, multifocal visual evoked potentials, and full-field visual evoked potentials of the fellow, non-symptomatic eye for subsequent multiple sclerosis development in patients with acute optic neuritis. Mult Scler, 27: 391–400. https://doi.org/10.1177/1352458520917924

 

  1. Sorensen PS, Sellebjerg F, Hartung HP, et al., 2020, The apparently milder course of multiple sclerosis: Changes in the diagnostic criteria, therapy and natural history. Brain, 143: 2637–2652. https://doi.org/10.1093/brain/awaa145

 

  1. Sati P, Oh J, Constable RT, et al., 2016, The central vein sign and its clinical evaluation for the diagnosis of multiple sclerosis: A consensus statement from the North American imaging in multiple sclerosis cooperative. Nat Rev Neurol, 12: 714–722. https://doi.org/10.1038/nrneurol.2016.166

 

  1. Van der Vuurst de Vries RM, Mescheriakova JY, Samijn JP, et al., 2018, Application of the 2017 revised McDonald criteria for Multiple Sclerosis to patients with a typical clinically isolated syndrome. JAMA Neurol, 75: 1392–1398. https://doi.org/10.1001/jamaneurol.2018.2160

 

  1. Lee DH, Peschke M, Utz KS, et al., 2019, Diagnostic value of the 2017 McDonald criteria in patients with a first demyelinating event suggestive of relapsing-remitting multiple sclerosis. Eur J Neurol, 26: 540–545. https://doi.org/10.1111/ene.13853

 

  1. Koch-Henriksen N, Thygesen LC, Stenager E, et al., 2018, Incidence of MS has increased markedly over six decades in Denmark particularly with late onset and in women. Neurology, 90: e1954–e1963. https://doi.org/10.1212/WNL.0000000000005612

 

  1. Petersen ER, Søndergaard HB, Laursen JH, et al., 2019, Smoking is associated with increased disease activity during natalizumab treatment in multiple sclerosis. Mult Scler, 25: 1298–1305. https://doi.org/10.1177/1352458518791753

 

  1. Solomon AJ, Marrie RA, Viswanathan S, et al., 2023, Global barriers to the diagnosis of multiple sclerosis: Data from the multiple sclerosis international federation atlas of MS, third edition. Neurology, 101: e624–e635. https://doi.org/10.1212/WNL.0000000000207481

 

  1. Chun BY, Kim JH, Jung YK, et al., 2021, Protective role of limitrin in experimental autoimmune optic neuritis. Invest Ophthalmol Vis Sci, 62: 8. https://doi.org/10.1167/iovs.62.9.8

 

  1. Winter A, Chwalisz B, 2020, MRI characteristics of NMO, MOG and MS related optic neuritis. Semin Ophthalmol, 35: 333–342. https://doi.org/10.1080/08820538.2020.1866027

 

  1. Çoban A, Düzel B, Tüzün E, et al., 2017, Investigation of the prognostic value of adipokines in multiple sclerosis. Mult Scler Relat Disord, 15: 11–14. https://doi.org/10.1016/j.msard.2017.04.006

 

  1. Pulido-Valdeolivas I, Andorrà M, Gómez-Andrés D, et al., 2020, Retinal and brain damage during multiple sclerosis course: Inflammatory activity is a key factor in the first 5 years. Sci Rep, 10: 13333. https://doi.org/10.1038/s41598-020-70255-z

 

  1. Alba-Arbalat S, Andorra M, Sanchez-Dalmau B, et al., 2021, In vivo molecular changes in the retina of patients with multiple sclerosis. Invest Ophthalmol Vis Sci, 62: 11. https://doi.org/10.1167/iovs.62.6.11

 

  1. Vural G, Gümüşyayla Ş, Deniz O, et al., 2019, Relationship between thiol-disulphide homeostasis and visual evoked potentials in patients with multiple sclerosis. Neurol Sci, 40: 385–391. https://doi.org/10.1007/s10072-018-3660-3

 

  1. Sadam H, Pihlak A, Jaago M, et al., 2021, Identification of two highly antigenic epitope markers predicting multiple sclerosis in optic neuritis patients. EBioMedicine, 64: 103211. https://doi.org/10.1016/j.ebiom.2021.103211

 

  1. Gharagozloo M, Smith MD, Jin J, et al., 2021, Complement component 3 from astrocytes mediates retinal ganglion cell loss during neuroinflammation. Acta Neuropathol, 142: 899–915. https://doi.org/10.1007/s00401-021-02366-4

 

  1. Liddelow SA, Guttenplan KA, Clarke LE, et al., 2017, Neurotoxic reactive astrocytes are induced by activated microglia. Nature, 541: 481–487. https://doi.org/10.1038/nature21029

 

  1. Roostaei T, Sadaghiani S, Mashhadi R, et al., 2019, Convergent effects of a functional C3 variant on brain atrophy, demyelination, and cognitive impairment in multiple sclerosis. Mult Scler, 25: 532–540.0 https://doi.org/10.1177/1352458518760715

 

  1. Jin J, Smith MD, Kersbergen CJ, et al., 2019, Glial pathology and retinal neurotoxicity in the anterior visual pathway in experimental autoimmune encephalomyelitis. Acta Neuropathol Commun, 7: 125. https://doi.org/10.1186/s40478-019-0767-6

 

  1. Wu Q, Miao X, Zhang J, et al., 2021, Astrocytic YAP protects the optic nerve and retina in an experimental autoimmune encephalomyelitis model through TGF-β signaling. Theranostics, 11: 8480–8499. https://doi.org/10.7150/thno.60031
Share
Back to top
Advanced Neurology, Electronic ISSN: 2810-9619 Print ISSN: 3060-8589, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept