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Latent microbial infections leading to myelin and axonal damage in multiple sclerosis: A narrative review

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Document Type : Review Article

Authors

1 School of Medicine, Tonekabon Branch, Islamic Azad University, Tonekabon, Iran

2 Department of Microbiology, School of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

3 Zoonoses Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran Department of Microbiology, Faculty of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran

4 Microbial Biotechnology Research Center, Iran University of Medical Sciences, Tehran, Iran

5 Iranian Reference Health Laboratory Research Center, Ministry of Health and Medical Education, Tehran, Iran

6 Infectious Diseases Research Center, Aja University of Medical Sciences, Tehran, Iran

Abstract

Background: Multiple sclerosis (MS) is a complex autoimmune disease characterized by chronic inflammation, demyelination, and axonal damage in the central nervous system (CNS). This review specifically aims to investigate the role of latent microbial infections-such as those caused by Epstein-Barr virus (EBV), Chlamydia pneumoniae, and others-in contributing to myelin and axon damage in MS.
Methods: We evaluated recent studies from PubMed, Google Scholar, and Scopus databases that focus on the relationship between latent microbial infections and MS pathogenesis.
Results: In MS, emerging evidence suggests that latent microbial infections play a significant role in triggering and perpetuating the inflammatory processes associated with the disease. The potential mechanisms by which these infections contribute to the pathogenesis of MS, highlighting the interplay between the immune system, microbial agents, and the CNS are evaluated. These include molecular mimicry, where similarities in sequence or structure between viral, bacterial, or self-peptides can activate autoreactive T or B cells through cross activation by pathogen-derived peptides, chronic inflammation triggered by persistent infection, leading to immune-mediated damage, and disruption of the blood-brain barrier, allowing microbial agents or immune cells to infiltrate the CNS.
Conclusion: This review underscores the critical role of latent microbial infections in MS pathogenesis. By elucidating these mechanisms, we provide new insights that could inform the development of innovative therapeutic interventions and preventive strategies for MS.

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References
  1. Piggott T, Nonino F, Baldin E, Filippini G, Rijke N, Schunemann H, et al. Multiple Sclerosis International Federation guideline methodology for off-label treatments for multiple sclerosis. Mult Scler J Exp Transl Clin 2021; 7(4): 20552173211051855.
  2. Goncalves JNC, Cortez P, Carvalho MS, Fraz+úo NM. A multivariate approach for multi-step demand forecasting in assembly industries: Empirical evidence from an automotive supply chain. Decision Support Systems 2021; 142: 113452.
  3. Nicholson TR, Carson A, Edwards MJ, Goldstein LH, Hallett M, Mildon B, et al. Outcome measures for functional neurological disorder: A review of the theoretical complexities. J Neuropsychiatry Clin Neurosci 2020; 32(1): 33-42.
  4. Lakin L, Davis BE, Binns CC, Currie KM, Rensel MR. Comprehensive approach to management of multiple sclerosis: addressing invisible symptoms-a narrative review. Neurol Ther 2021; 10(1): 75-98.
  5. Correale J, Marrodan M, Ysrraelit MC. Mechanisms of neurodegeneration and axonal dysfunction in progressive multiple sclerosis. Biomedicines 2019; 7(1): 14.
  6. Milo R, Korczyn AD, Manouchehri N, Stuve O. The temporal and causal relationship between inflammation and neurodegeneration in multiple sclerosis. Mult Scler 2020; 26(8): 876-86.
  7. Franklin RJ, Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008; 9(11): 839-55.
  8. Lassmann H. Pathogenic mechanisms associated with different clinical courses of multiple sclerosis. Front Immunol 2018; 9: 3116.
  9. Frischer JM, Bramow S, Dal-Bianco A, Lucchinetti CF, Rauschka H, Schmidbauer M, et al. The relation between inflammation and neurodegeneration in multiple sclerosis brains. Brain 2009; 132(Pt 5): 1175-89.
  10. Hauser SL, Oksenberg JR. The neurobiology of multiple sclerosis: Genes, inflammation, and neurodegeneration. Neuron 2006; 52(1): 61-76.
  11. Wekerle H, Lassmann H. The immunology of inflammatory demyelinating disease. In: Compston A, Confavreux C, Lassmann H, McDonald I, Miller D, Noseworthy J, et al., editors. McAlpine's Multiple Sclerosis. 4thEdinburgh, UK: Churchill Livingstone; 2006. p. 491-555.
  12. Venigalla SSK, Premakumar S, Janakiraman V. A possible role for autoimmunity through molecular mimicry in alphavirus mediated arthritis. Sci Rep 2020; 10(1): 938.
  13. Lucchinetti CF, Mandler RN, McGavern D, Bruck W, Gleich G, Ransohoff RM, et al. A role for humoral mechanisms in the pathogenesis of Devic's neuromyelitis optica. Brain 2002; 125(Pt 7): 1450-61.
  14. Hoftberger R, Lassmann H, Berger T, Reindl M. Pathogenic autoantibodies in multiple sclerosis - from a simple idea to a complex concept. Nat Rev Neurol 2022; 18(11): 681-8.
  15. Kim JS, Soto-Diaz K, Bingham TW, Steelman AJ, Das A. Role of omega-3 endocannabinoids in the modulation of T-cell activity in a multiple sclerosis experimental autoimmune encephalomyelitis (EAE) model. J Biol Chem 2023; 299(2): 102886.
  16. Tiwari S, Lapierre J, Ojha CR, Martins K, Parira T, Dutta RK, et al. Signaling pathways and therapeutic perspectives related to environmental factors associated with multiple sclerosis. J Neurosci Res 2018; 96(12): 1831-46.
  17. Marrodan M, Alessandro L, Farez MF, Correale J. The role of infections in multiple sclerosis. Mult Scler 2019; 25(7): 891-901.
  18. Sundaresan B, Shirafkan F, Ripperger K, Rattay K. The Role of Viral Infections in the Onset of Autoimmune Diseases. Viruses 2023; 15(3): 782.
  19. Moudgil KD. Viewing autoimmune pathogenesis from the perspective of antigen processing and determinant hierarchy. Crit Rev Immunol 2020; 40(4): 329-39.
  20. Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 2009; 9(6): 393-407.
  21. Tarlinton RE, Martynova E, Rizvanov AA, Khaiboullina S, Verma S. Role of viruses in the pathogenesis of multiple sclerosis. Viruses 2020; 12(6): 643.
  22. Soldan SS, Lieberman PM. Epstein-Barr virus and multiple sclerosis. Nat Rev Microbiol 2023; 21(1): 51-64.
  23. Maciak K, Pietrasik S, Dziedzic A, Redlicka J, Saluk-Bijak J, Bijak M, et al. Th17-related cytokines as potential discriminatory markers between neuromyelitis optica (Devic's Disease) and multiple sclerosis-a review. Int J Mol Sci 2021; 22(16): 8946.
  24. Getts DR, Spiteri A, King NJC, Miller SD. Chapter 21 - microbial infection as a trigger of T-Cell Autoimmunity. In: Rose NR, Mackay IR, editors. The autoimmune diseases. 6th Academic Press; 2020. p. 363-74.
  25. Venkatesan A, Johnson RT. Infections and multiple sclerosis. Handb Clin Neurol 2014; 122: 151-71.
  26. Mangale V, McIntyre LL, Walsh CM, Loring JF, Lane TE. Promoting remyelination through cell transplantation therapies in a model of viral-induced neurodegenerative disease. Dev Dyn 2019; 248(1): 43-52.
  27. Dinarello CA. Proinflammatory cytokines. Chest 2000; 118(2): 503-8.
  28. Michalickova D, Sima M, Slanar O. New insights in the mechanisms of impaired redox signaling and its interplay with inflammation and immunity in multiple sclerosis. Physiol Res 2020; 69(1): 1-19.
  29. van Langelaar LJ, Rijvers L, Smolders J, van Luijn MM. B and T cells driving multiple sclerosis: identity, mechanisms and potential triggers. Front Immunol 2020; 11: 760.
  30. Schloder J, Shahneh F, Schneider FJ, Wieschendorf B. Boosting regulatory T cell function for the treatment of autoimmune diseases - That's only half the battle! Front Immunol 2022; 13: 973813.
  31. Verma ND, Lam AD, Chiu C, Tran GT, Hall BM, Hodgkinson SJ. Multiple sclerosis patients have reduced resting and increased activated CD4(+)CD25(+)FOXP3(+)T regulatory cells. Sci Rep 2021; 11(1): 10476.
  32. Saez-Calveras N, Stuve O. The role of the complement system in Multiple Sclerosis: A review. Front Immunol 2022; 13: 970486.
  33. Segarra M, Aburto MR, Acker-Palmer A. Blood-brain barrier dynamics to maintain brain homeostasis. Trends Neurosci 2021; 44(5): 393-405.
  34. Tran VTA, Lee LP, Cho H. Neuroinflammation in neurodegeneration via microbial infections. Front Immunol 2022; 13: 907804.
  35. Cai Z, Qiao PF, Wan CQ, Cai M, Zhou NK, Li Q. Role of blood-brain barrier in Alzheimer's Disease. J Alzheimers Dis 2018; 63(4): 1223-34.
  36. Dando SJ, Mackay-Sim A, Norton R, Currie BJ, St John JA, Ekberg JA, 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.
  37. da Fonseca AC, Matias D, Garcia C, Amaral R, Geraldo LH, Freitas C, et al. The impact of microglial activation on blood-brain barrier in brain diseases. Front Cell Neurosci 2014; 8: 362.
  38. Liu Q, Gao Y, Zhang B, Sun F, Yang Q, Liu Y, et al. Cytokine profiles in cerebrospinal fluid of patients with meningitis at a tertiary general hospital in China. J Microbiol Immunol Infect 2020; 53(2): 216-24.
  39. Gerhauser I, Hansmann F, Ciurkiewicz M, Loscher W, Beineke A. Facets of Theiler's murine encephalomyelitis virus-induced diseases: an update. Int J Mol Sci 2019; 20(2).
  40. Muri L, Leppert D, Grandgirard D, Leib SL. MMPs and ADAMs in neurological infectious diseases and multiple sclerosis. Cell Mol Life Sci 2019; 76(16): 3097-116.
  41. Krueger M, Mages B, Hobusch C, Michalski D. Endothelial edema precedes blood-brain barrier breakdown in early time points after experimental focal cerebral ischemia. Acta Neuropathol Commun 2019; 7(1): 17.
  42. Alvarez JI, Katayama T, Prat A. Glial influence on the blood brain barrier. Glia 2013; 61(12): 1939-58.
  43. Gay F. Bacterial toxins and Multiple Sclerosis. J Neurol Sci 2007; 262(1-2): 105-12.
  44. Chaoprasid P, Dersch P. The Cytotoxic Necrotizing Factors (CNFs)-A Family of Rho GTPase-Activating Bacterial Exotoxins. Toxins (Basel) 2021; 13(12).
  45. Takata F, Nakagawa S, Matsumoto J, Dohgu S. Blood-brain barrier dysfunction amplifies the development of neuroinflammation: Understanding of Cellular events in brain microvascular endothelial cells for prevention and treatment of BBB dysfunction. Front Cell Neurosci 2021; 15: 661838.
  46. Roe K. A latent pathogen infection classification system that would significantly increase healthcare safety. Immunol Res 2023; 71(5): 673-7.
  47. Khabibullina NF, Kutuzova DM, Burmistrova IA, Lyadova IV. The biological and clinical aspects of a latent tuberculosis infection. Trop Med Infect Dis 2022; 7(3): 48.
  48. Landry RL, Embers ME. The probable infectious origin of multiple sclerosis. NeuroSci 2023; 4(3): 211-34.
  49. Cossu D, Yokoyama K, Hattori N. Bacteria-host interactions in multiple sclerosis. Front Microbiol 2018; 9: 2966.
  50. Bjornevik K, Munz C, Cohen JI, Ascherio A. Epstein-Barr virus as a leading cause of multiple sclerosis: mechanisms and implications. Nat Rev Neurol 2023; 19(3): 160-71.
  51. Kakalacheva K, Munz C, Lunemann JD. Viral triggers of multiple sclerosis. Biochim Biophys Acta 2011; 1812(2): 132-40.
  52. Rosella M, Carmela R, Roberta R, Grazia M, Maria CB, Silvia R, et al. Viruses and neuroinflammation in multiple sclerosis. Neuroimmunology and Neuroinflammation 2021; 8: -269.
  53. Shi T, Huang L, Tian J. Prevalence of Epstein-Barr Viral DNA among children at a single hospital in Suzhou, China. J Pediatr (Rio J) 2022; 98(2): 142-6.
  54. Ascherio A, Munger KL. Epstein-Barr virus infection and multiple sclerosis: a review. J Neuroimmune Pharmacol 2010; 5(3): 271-7.
  55. Guan Y, Jakimovski D, Ramanathan M, Weinstock-Guttman B, Zivadinov R. The role of Epstein-Barr virus in multiple sclerosis: from molecular pathophysiology to in vivo imaging. Neural Regen Res 2019; 14(3): 373-86.
  56. Thomas OG, Rickinson A, Palendira U. Epstein-Barr virus and multiple sclerosis: moving from questions of association to questions of mechanism. Clin Transl Immunology 2023; 12(5): e1451.
  57. Serafini B, Rosicarelli B, Veroni C, Mazzola GA, Aloisi F. Epstein-Barr virus-specific CD8 T cells selectively infiltrate the brain in multiple sclerosis and interact locally with virus-infected cells: Clue for a virus-driven immunopathological mechanism. J Virol 2019; 93(24): 00980-19.
  58. Hedstrom AK. Risk factors for multiple sclerosis in the context of Epstein-Barr virus infection. Front Immunol 2023; 14: 1212676.
  59. Bjornevik K, Cortese M, Healy BC, Kuhle J, Mina MJ, Leng Y, et al. Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis. Science 2022; 375(6578): 296-301.
  60. Bar-Or A, Pender MP, Khanna R, Steinman L, Hartung HP, Maniar T, et al. Epstein-Barr virus in multiple sclerosis: Theory and emerging immunotherapies. Trends Mol Med 2020; 26(3): 296-310.
  61. Sedighi S, Gholizadeh O, Yasamineh S, Akbarzadeh S, Amini P, Favakehi P, et al. Comprehensive investigations relationship between viral infections and multiple sclerosis pathogenesis. Curr Microbiol 2022; 80(1): 15.
  62. Veroni C, Aloisi F. The CD8 T Cell-Epstein-Barr Virus-B cell trialogue: A central issue in multiple sclerosis pathogenesis. Front Immunol 2021; 12: 665718.
  63. Kakalacheva K, Munz C, Lunemann JD. Viral triggers of multiple sclerosis. Biochim Biophys Acta 2011; 1812(2): 132-40.
  64. Voumvourakis KI, Fragkou PC, Kitsos DK, Foska K, Chondrogianni M, Tsiodras S. Human herpesvirus 6 infection as a trigger of multiple sclerosis: An update of recent literature. BMC Neurol 2022; 22(1): 57.
  65. Keyvani H, Zahednasab H, Aljanabi HAA, Asadi M, Mirzaei R, Esghaei M, et al. The role of human herpesvirus-6 and inflammatory markers in the pathogenesis of multiple sclerosis. J Neuroimmunol 2020; 346: 577313.
  66. Jeanne Billioux B, Alvarez Lafuente R, Jacobson S. HHV-6 and multiple sclerosis. Human herpesviruses HHV-6A, HHV-6B & HHV-7 2014: 123-42.
  67. Leibovitch EC, Jacobson S. Evidence linking HHV-6 with multiple sclerosis: An update. Curr Opin Virol 2014; 9: 127-33.
  68. Morris G, Maes M, Murdjeva M, Puri BK. Do human endogenous retroviruses contribute to multiple sclerosis, and if so, how? Mol Neurobiol 2019; 56(4): 2590-605.
  69. Donati D. Viral infections and multiple sclerosis. Drug Discov Today Dis Models 2020; 32: 27-33.
  70. Uzun N. Chlamydia infection's role in neurological diseases. In: Sarier M, editor. Chlamydia - secret enemy from past to present. Intechopen [Online 2023]. [cited 2023 Apr 20]; Available from: URL: https://www.intechopen.com/chapters/86946
  71. Pastor Bandeira I, Silva C, Martin M, Silva GF, Parolin L, Melo L, et al. Latent tuberculosis infection in patients with multiple sclerosis [Preprints]. 2020.
  72. Esmailkhani A, Akhi MT, Sadeghi J, Niknafs B, Zahedi BA, Farzadi L, et al. Assessing the prevalence of Staphylococcus aureus in infertile male patients in Tabriz, northwest Iran. Int J Reprod Biomed 2018; 16(7): 469-74.
  73. Zarghami A, Li Y, Claflin SB, van der Mei I, Taylor BV. Role of environmental factors in multiple sclerosis. Expert Rev Neurother 2021; 21(12): 1389-408.
  74. Correale J, Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol 2007; 61(2): 97-108.
  75. Karpus WJ. Cytokines and chemokines in the pathogenesis of experimental autoimmune encephalomyelitis. J Immunol 2020; 204(2): 316-26.
  76. Arjmandi D, Graeili Z, Mohammadi P, Arshadi M, Jafari TM, Ardekani A, et al. Chlamydia pneumonia infection and risk of multiple sclerosis: A meta-analysis. Mult Scler Relat Disord 2023; 77: 104862.
  77. Sriram S, Stratton CW, Yao S, Tharp A, Ding L, Bannan JD, et al. Chlamydia pneumoniae infection of the central nervous system in multiple sclerosis. Ann Neurol 1999; 46(1): 6-14.
  78. Doran KS, Banerjee A, Disson O, Lecuit M. Concepts and mechanisms: crossing host barriers. Cold Spring Harb Perspect Med 2013; 3(7): a010090.
  79. Kazemi S, Lashtoo Aghaee B, Soltanian AR, Mazdeh M, Taheri M, Alikhani MY. Investigation of chlamydia pneumoniae infection in patients with multiple sclerosis: A case-control study. Avicenna J Clin Microbiol Infect 2020; 7(2): 36-9.
  80. Woods JJ, Skelding KA, Martin KL, Aryal R, Sontag E, Johnstone DM, et al. Assessment of evidence for or against contributions of Chlamydia pneumoniae infections to Alzheimer's disease etiology. Brain Behav Immun 2020; 83: 22-32.
  81. Libbey JE, Cusick MF, Fujinami RS. Role of pathogens in multiple sclerosis. Int Rev Immunol 2014; 33(4): 266-83.
  82. Huang Y, Wang QL, Cheng DD, Xu WT, Lu NH. Adhesion and invasion of gastric mucosa epithelial cells by Helicobacter pylori. Front Cell Infect Microbiol 2016; 6: 159.
  83. Efthymiou G, Dardiotis E, Liaskos C, Marou E, Tsimourtou V, Rigopoulou EI, et al. Immune responses against Helicobacter pylori-specific antigens differentiate relapsing remitting from secondary progressive multiple sclerosis. Sci Rep 2017; 7(1): 7929.
  84. Mirmosayyeb O, Barzegar M, Nehzat N, Najdaghi S, Ansari B, Shaygannejad V. Association of helicobacter pylori with multiple sclerosis: Protective or risk factor? Curr J Neurol 2020; 19(2): 59-66.
  85. Gavalas E, Kountouras J, Boziki M, Zavos C, Polyzos SA, Vlachaki E, et al. Relationship between Helicobacter pylori infection and multiple sclerosis. Ann Gastroenterol 2015; 28(3): 353-6.
  86. Cook KW, Crooks J, Hussain K, O'Brien K, Braitch M, Kareem H, et al. Helicobacter pylori infection reduces disease severity in an experimental model of multiple sclerosis. Front Microbiol 2015; 6: 52.
  87. Kountouras J, Zavos C, Polyzos SA, Deretzi G. The gut-brain axis: Interactions between Helicobacter pylori and enteric and central nervous systems. Ann Gastroenterol 2015; 28(4): 506.
  88. Whiteside SK, Snook JP, Ma Y, Sonderegger FL, Fisher C, Petersen C, et al. IL-10 Deficiency reveals a role for TLR2-dependent bystander activation of T cells in Lyme Arthritis. J Immunol 2018; 200(4): 1457-70.
  89. Tracy KE, Baumgarth N. Borrelia burgdorferi manipulates innate and adaptive immunity to establish persistence in rodent reservoir hosts. Front Immunol 2017; 8: 116.
  90. Chmielewska-Badora J, Cisak E, Dutkiewicz J. Lyme borreliosis and multiple sclerosis: any connection? A seroepidemic study. Ann Agric Environ Med 2000; 7(2): 141-3.
  91. Chai Q, Zhang Y, Liu CH. Mycobacterium tuberculosis: An adaptable pathogen associated with multiple human diseases. Front Cell Infect Microbiol 2018; 8: 158.
  92. Kiazyk S, Ball TB. Latent tuberculosis infection: An overview. Can Commun Dis Rep 2017; 43(3-4): 62-6.
  93. Cossu D, Yokoyama K, Hattori N. Conflicting role of mycobacterium species in multiple sclerosis. Front Neurol 2017; 8: 216.
  94. Lehmann D, Ben-Nun A. Bacterial agents protect against autoimmune disease. I. Mice pre-exposed to Bordetella pertussis or Mycobacterium tuberculosis are highly refractory to induction of experimental autoimmune encephalomyelitis. J Autoimmun 1992; 5(6): 675-90.
  95. Salvetti M, Ristori G, Buttinelli C, Fiori P, Falcone M, Britton W, et al. The immune response to mycobacterial 70-kDa heat shock proteins frequently involves autoreactive T cells and is quantitatively disregulated in multiple sclerosis. J Neuroimmunol 1996; 65(2): 143-53.
  96. Liverani E, Scaioli E, Cardamone C, Dal MP, Belluzzi A. Mycobacterium avium subspecies paratuberculosis in the etiology of Crohn's disease, cause or epiphenomenon? World J Gastroenterol 2014; 20(36): 13060-70.
  97. Cossu D, Mameli G, Galleri G, Cocco E, Masala S, Frau J, et al. Human interferon regulatory factor 5 homologous epitopes of Epstein-Barr virus and Mycobacterium avium subsp. paratuberculosis induce a specific humoral and cellular immune response in multiple sclerosis patients. Mult Scler 2015; 21(8): 984-95.
  98. Mameli G, Cocco E, Frau J, Marrosu MG, Sechi LA. Epstein Barr Virus and Mycobacterium avium subsp. Paratuberculosis peptides are recognized in sera and cerebrospinal fluid of MS patients. Sci Rep 2016; 6: 22401.
  99. Arsenault RJ, Li Y, Maattanen P, Scruten E, Doig K, Potter A, et al. Altered Toll-like receptor 9 signaling in Mycobacterium avium subsp. paratuberculosis-infected bovine monocytes reveals potential therapeutic targets. Infect Immun 2013; 81(1): 226-37.
  100. Cossu D, Masala S, Sechi LA. A Sardinian map for multiple sclerosis. Future Microbiol 2013; 8(2): 223-32.
  101. Ramos M, Pisa D, Molina S, Rabano A, Juarranz A, Carrasco L. Fungal infection in patients with multiple sclerosis. The Open Mycology Journal 2008; 2(1): 22-8.
  102. Mangalam AK. Fungal microbiome and multiple sclerosis: The not-so-new kid on the block. EBioMedicine 2021; 72: 103621.
  103. Tanasescu R, Tench CR, Constantinescu CS, Telford G, Singh S, Frakich N, et al. Hookworm treatment for relapsing multiple sclerosis: A randomized double-blinded placebo-controlled trial. JAMA Neurol 2020; 77(9): 1089-98.
  104. Yordanova IA, Ebner F, Schulz AR, Steinfelder S, Rosche B, Bolze A, et al. The worm-specific immune response in multiple sclerosis patients receiving controlled Trichuris suis Ova immunotherapy. Life (Basel) 2021; 11(2): 101.
  105. Scotto R, Reia A, Buonomo AR, Moccia M, Viceconte G, Pisano E, et al. Risk of invasive fungal infections among patients treated with disease modifying treatments for multiple sclerosis: A comprehensive review. Expert Opin Drug Saf 2021; 20(8): 925-36.
  106. Benito-Leon J, Laurence M. The role of fungi in the etiology of multiple sclerosis. Front Neurol 2017; 8: 535.
  107. Goldszmid RS, Caspar P, Rivollier A, White S, Dzutsev A, Hieny S, et al. NK cell-derived interferon-gamma orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 2012; 36(6): 1047-59.
  108. Keighobadi M, Alokandeh ND, Baghbanian SM, Karimi N. The role of Toxoplasma gondii in multiple sclerosis: A matched case-control study. Neurology Asia 2021; 26(2): 333-9.
  109. Nicoletti A, Cicero CE, Giuliano L, Todaro V, Lo Fermo S, Chisari C, et al. Toxoplasma gondii and multiple sclerosis: A population-based case-control study. Sci Rep 2020; 10(1): 18855.
  110. Rahnama M, Asgari Q, Petramfar P , Tasa D, Hemati V, et al. The role of Toxoplasma gondii infection among multiple sclerosis patient compared to ordinary people in south of Iran: A Case-Control Study. Mod Care J 2020; 17(3): e105090.
  111. Marignier R, Hacohen Y, Cobo-Calvo A, Probstel AK, Aktas O, Alexopoulos H, et al. Myelin-oligodendrocyte glycoprotein antibody-associated disease. Lancet Neurol 2021; 20(9): 762-72.
  112. Sotgiu S, Sannella AR, Conti B, Arru G, Fois ML, Sanna A, et al. Multiple sclerosis and anti-Plasmodium falciparum innate immune response. J Neuroimmunol 2007; 185(1-2): 201-7.
  113. Belbasis L, Bellou V, Evangelou E, Tzoulaki I. Environmental factors and risk of multiple sclerosis: Findings from meta-analyses and Mendelian randomization studies. Mult Scler 2020; 26(4): 397-404.
  114. Omerhoca S, Akkas SY, Icen NK. Multiple sclerosis: Diagnosis and differential diagnosis. Noro Psikiyatr Ars 2018; 55(Suppl 1): S1-S9.
  115. Asouri M, Sahraian MA, Karimpoor M, Fattahi S, Motamed N, Doosti R, et al. Molecular detection of epstein-barr virus, human herpes virus 6, cytomegalovirus, and hepatitis B virus in patients with multiple sclerosis. Middle East J Dig Dis 2020; 12(3): 171-7.
  116. Ruprecht K. The role of Epstein-Barr virus in the etiology of multiple sclerosis: A current review. Expert Rev Clin Immunol 2020; 16(12): 1143-57.
  117. Khalesi Z, Tamrchi V, Razizadeh MH, Letafati A, Moradi P, Habibi A, et al. Association between human herpesviruses and multiple sclerosis: A systematic review and meta-analysis. Microb Pathog 2023; 177: 106031.
  118. Jakhmola S, Upadhyay A, Jain K, Mishra A, Jha HC. Herpesviruses and the hidden links to Multiple Sclerosis neuropathology. J Neuroimmunol 2021; 358: 577636.
  119. Xu Y, Hiyoshi A, Smith KA, Piehl F, Olsson T, Fall K, et al. Association of infectious mononucleosis in childhood and adolescence with risk for a subsequent multiple sclerosis diagnosis among siblings. JAMA Netw Open 2021; 4(10): e2124932.
  120. Perlejewski K, Bukowska-Osko I, Rydzanicz M, Dzieciatkowski T, Zakrzewska-Pniewska B, Podlecka-Pietowska A, et al. Search for viral agents in cerebrospinal fluid in patients with multiple sclerosis using real-time PCR and metagenomics. PLoS One 2020; 15(10): e0240601.
  121. Pagani CF, Curbelo MC, Vazquez G, Sedeno L, Steinberg J, Carra A, et al. Application of the 2017 McDonald criteria for the diagnosis of multiple sclerosis after a first demyelinating event in patients from Argentina. Mult Scler Relat Disord 2020; 41: 102043.
  122. Tan IL, McArthur JC, Clifford DB, Major EO, Nath A. Immune reconstitution inflammatory syndrome in natalizumab-associated PML. Neurology 2011; 77(11): 1061-7.
  123. Messe A, Caplain S, Paradot G, Garrigue D, Mineo JF, Soto AG, et al. Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment. Hum Brain Mapp 2011; 32(6): 999-1011.
  124. Shah R, Bag AK, Chapman PR, Cure JK. Imaging manifestations of progressive multifocal leukoencephalopathy. Clin Radiol 2010; 65(6): 431-9.
  125. Lycke J. Trials of antivirals in the treatment of multiple sclerosis. Acta Neurol Scand 2017; 136 Suppl 201: 45-8.
  126. Yang JH, Rempe T, Whitmire N, Dunn-Pirio A, Graves JS. Therapeutic advances in multiple sclerosis. Front Neurol 2022; 13: 824926.
  127. Giovannoni G. Personalized medicine in multiple sclerosis. Neurodegener Dis Manag 2017; 7(6s): 13-7.
  128. Hosseinzadeh A, Iranpour S, Adineh HA, Aliyari R. Antibiotic use and multiple sclerosis: A systematic review and meta-analysis. Mult Scler Relat Disord 2023; 75: 104765.
  129. Mendes A, Sa MJ. Classical immunomodulatory therapy in multiple sclerosis: How it acts, how it works. Arq Neuropsiquiatr 2011; 69(3): 536-43.
  130. Rahmani M, Negro Alvarez SE, Hernandez EB. The potential use of tetracyclines in neurodegenerative diseases and the role of nano-based drug delivery systems. Eur J Pharm Sci 2022; 175: 106237.
  131. Wang D, Lu Z, Hu L, Zhang Y, Hu X. Macrolide antibiotics aggravate experimental autoimmune encephalomyelitis and inhibit inducible nitric oxide synthase. Immunol Invest 2009; 38(7): 602-12.
  132. Dumitrescu L, Papathanasiou A, Coclitu C, Constantinescu CS, Popescu BO, Tanasescu R. Beta interferons as immunotherapy in multiple sclerosis: a new outlook on a classic drug during the COVID-19 pandemic. QJM 2021; 114(10): 691-7.
  133. Bourque J, Hawiger D. Current and future immunotherapies for multiple sclerosis. Mo Med 2021; 118(4): 334-9.
  134. Freedman MS, Selchen D, Prat A, Giacomini PS. Managing multiple sclerosis: Treatment initiation, modification, and sequencing. Can J Neurol Sci 2018; 45(5): 489-503.
  135. Wingerchuk DM, Carter JL. Multiple sclerosis: current and emerging disease-modifying therapies and treatment strategies. Mayo Clin Proc 2014; 89(2): 225-40.
  136. Greenberg BM, Calabresi PA. Future research directions in multiple sclerosis therapies. Semin Neurol 2008; 28(1): 121-7.
Current Journal of Neurology

Articles in Press, Accepted Manuscript
Available Online from 25 December 2024
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