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Semin Neurol 2023; 43(02): 229-250
DOI: 10.1055/s-0043-1767713
Review Article

Central Nervous System Neuroimmunologic Complications of COVID-19

Kathryn B. Holroyd 
1   Department of Neurology, Brigham and Women's Hospital, Boston, Massachusetts
,
Sarah E. Conway
1   Department of Neurology, Brigham and Women's Hospital, Boston, Massachusetts
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Abstract

Autoimmune disorders of the central nervous system following COVID-19 infection include multiple sclerosis (MS), neuromyelitis optica spectrum disorder, myelin oligodendrocyte glycoprotein antibody-associated disease, autoimmune encephalitis, acute disseminated encephalomyelitis, and other less common neuroimmunologic disorders. In general, these disorders are rare and likely represent postinfectious phenomena rather than direct consequences of the SARS-CoV-2 virus itself. The impact of COVID-19 infection on patients with preexisting neuroinflammatory disorders depends on both the disorder and disease-modifying therapy use. Patients with MS do not have an increased risk for severe COVID-19, though patients on anti-CD20 therapies may have worse clinical outcomes and attenuated humoral response to vaccination. Data are limited for other neuroinflammatory disorders, but known risk factors such as older age and medical comorbidities likely play a role. Prophylaxis and treatment for COVID-19 should be considered in patients with preexisting neuroinflammatory disorders at high risk for developing severe COVID-19.

Keywords

COVID-19 - multiple sclerosis - neuromyelitis optica - neuroinflammation - encephalitis


Publikationsverlauf

Artikel online veröffentlicht:
20. April 2023

© 2023. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Mao L, Jin H, Wang M. et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol 2020; 77 (06) 683-690
    CrossrefPubMedGoogle Scholar
  • 2 Zhou S, Jones-Lopez EC, Soneji DJ, Azevedo CJ, Patel VR. Myelin oligodendrocyte glycoprotein antibody-associated optic neuritis and myelitis in COVID-19. J Neuroophthalmol 2020; 40 (03) 398-402
    CrossrefPubMedGoogle Scholar
  • 3 Corrêa DG, de Souza Lima FC, da Cruz Bezerra D, Coutinho AC, Hygino da Cruz LC. COVID-19 associated with encephalomyeloradiculitis and positive anti-aquaporin-4 antibodies: Cause or coincidence?. Mult Scler 2021; 27 (06) 973-976
    CrossrefPubMedGoogle Scholar
  • 4 Ismail II, Salama S. Association of CNS demyelination and COVID-19 infection: an updated systematic review. J Neurol 2022; 269 (02) 541-576
    CrossrefPubMedGoogle Scholar
  • 5 WHO Team. Weekly Epidemiological Update on COVID-19 - June 29, 2021. World Health Organization; 2021
    Google Scholar
  • 6 Normandin E, Holroyd KB, Collens SI. et al. Intrathecal inflammatory responses in the absence of SARS-CoV-2 nucleic acid in the CSF of COVID-19 hospitalized patients. J Neurol Sci 2021; 430: 120023
    CrossrefPubMedGoogle Scholar
  • 7 Solomon IH, Normandin E, Bhattacharyya S. et al. Neuropathological features of COVID-19. N Engl J Med 2020; 383 (10) 989-992
    CrossrefPubMedGoogle Scholar
  • 8 Manzano GS, McEntire CRS, Martinez-Lage M, Mateen FJ, Hutto SK. Acute disseminated encephalomyelitis and acute hemorrhagic leukoencephalitis following COVID-19: systematic review and meta-synthesis. Neurol Neuroimmunol Neuroinflamm 2021; 8 (06) e1080
    CrossrefPubMedGoogle Scholar
  • 9 Marino Gammazza A, Légaré S, Lo Bosco G. et al. Molecular mimicry in the post-COVID-19 signs and symptoms of neurovegetative disorders?. Lancet Microbe 2021; 2 (03) e94
    CrossrefPubMedGoogle Scholar
  • 10 Song E, Bartley CM, Chow RD. et al. Divergent and self-reactive immune responses in the CNS of COVID-19 patients with neurological symptoms. Cell Rep Med 2021; 2 (05) 100288
    CrossrefPubMedGoogle Scholar
  • 11 Spudich S, Nath A. Nervous system consequences of COVID-19. Science 2022; 375 (6578): 267-269
    CrossrefPubMedGoogle Scholar
  • 12 Lima M, Aloizou AM, Siokas V. et al. Coronaviruses and their relationship with multiple sclerosis: is the prevalence of multiple sclerosis going to increase after the COVID-19 pandemia?. Rev Neurosci 2022; 33 (07) 703-720
    CrossrefPubMedGoogle Scholar
  • 13 Walton C, King R, Rechtman L. et al. Rising prevalence of multiple sclerosis worldwide: insights from the Atlas of MS, third edition. Mult Scler 2020; 26 (14) 1816-1821
    CrossrefPubMedGoogle Scholar
  • 14 Bjornevik K, Cortese M, Healy BC. et al. Longitudinal analysis reveals high prevalence of Epstein-Barr virus associated with multiple sclerosis. Science 2022; 375 (6578): 296-301
    CrossrefPubMedGoogle Scholar
  • 15 Confavreux C. Infections and the risk of relapse in multiple sclerosis. Brain 2002; 125 (Pt 5): 933-934
    CrossrefPubMedGoogle Scholar
  • 16 Palao M, Fernández-Díaz E, Gracia-Gil J, Romero-Sánchez CM, Díaz-Maroto I, Segura T. Multiple sclerosis following SARS-CoV-2 infection. Mult Scler Relat Disord 2020; 45: 102377
    CrossrefPubMedGoogle Scholar
  • 17 Yavari F, Raji S, Moradi F, Saeidi M. Demyelinating changes alike to multiple sclerosis: a case report of rare manifestations of COVID-19. Case Rep Neurol Med 2020; 2020: 6682251
    PubMedGoogle Scholar
  • 18 Moore L, Ghannam M, Manousakis G. A first presentation of multiple sclerosis with concurrent COVID-19 infection. eNeurologicalSci 2021; 22: 100299
    CrossrefPubMedGoogle Scholar
  • 19 Sarwar S, Rogers S, Mohamed AS. et al. Multiple sclerosis following SARS-CoV-2 infection: a case report and literature review. Cureus 2021; 13 (10) e19036
    PubMedGoogle Scholar
  • 20 Ibrahim Ismail I, Al-Hashel J, Alroughani R, Farouk Ahmed S. A case report of multiple sclerosis after COVID-19 infection: causality or coincidence?. Neuroimmunology Reports 2021; 1: 100008
    CrossrefPubMedGoogle Scholar
  • 21 Khair AM, Nikam R, Husain S, Ortiz M, Kaur G. Para and post-COVID-19 CNS acute demyelinating disorders in children: a case series on expanding the spectrum of clinical and radiological characteristics. Cureus 2022; 14 (03) e23405
    PubMedGoogle Scholar
  • 22 Pignolo A, Aprile M, Gagliardo C. et al. Clinical onset and multiple sclerosis relapse after SARS-CoV-2 infection. Neurol Int 2021; 13 (04) 695-700
    CrossrefPubMedGoogle Scholar
  • 23 Narayan R, Simpson A, Fritsche K. et al. MOG antibody disease: a review of MOG antibody seropositive neuromyelitis optica spectrum disorder. Mult Scler Relat Disord 2018; 25: 66-72
    CrossrefPubMedGoogle Scholar
  • 24 Kogure C, Kikushima W, Fukuda Y. et al. Myelin oligodendrocyte glycoprotein antibody-associated optic neuritis in a COVID-19 patient: a case report. Medicine (Baltimore) 2021; 100 (19) e25865
    CrossrefPubMedGoogle Scholar
  • 25 Rojas-Correa DX, Reche-Sainz JA, Insausti-García A, Calleja-García C, Ferro-Osuna M. Post COVID-19 myelin oligodendrocyte glycoprotein antibody-associated optic neuritis. Neuroophthalmology 2021; 46 (02) 115-121
    CrossrefPubMedGoogle Scholar
  • 26 de Ruijter NS, Kramer G, Gons RAR, Hengstman GJD. Neuromyelitis optica spectrum disorder after presumed coronavirus (COVID-19) infection: a case report. Mult Scler Relat Disord 2020; 46: 102474
    CrossrefPubMedGoogle Scholar
  • 27 Sawalha K, Adeodokun S, Kamoga GR. COVID-19-induced acute bilateral optic neuritis. J Investig Med High Impact Case Rep 2020; 8: 2324709620976018
    CrossrefPubMedGoogle Scholar
  • 28 Khan A, Panwala H, Ramadoss D, Khubchandani R. Myelin oligodendrocyte glycoprotein (MOG) antibody disease in a 11 year old with COVID-19 infection. Indian J Pediatr 2021; 88 (05) 488-489
    CrossrefPubMedGoogle Scholar
  • 29 Sinha R, Wander A, Kapoor A, Yadav R, Kumar A, Gulati S. Acute demyelinating syndrome (MOG antibody positive) associated with COVID-19 infection: a widening spectrum. Clin Pediatr (Phila) 2021; 60 (13) 501-503
    CrossrefPubMedGoogle Scholar
  • 30 Jumah M, Rahman F, Figgie M. et al. COVID-19, HHV6 and MOG antibody: a perfect storm. J Neuroimmunol 2021; 353: 577521
    CrossrefPubMedGoogle Scholar
  • 31 Dias da Costa M, Leal Rato M, Cruz D, Valadas A, Antunes AP, Albuquerque L. Longitudinally extensive transverse myelitis with anti-myelin oligodendrocyte glycoprotein antibodies following SARS-CoV-2 infection. J Neuroimmunol 2021; 361: 577739
    CrossrefPubMedGoogle Scholar
  • 32 Yang E, Husein A, Martinez-Perez J, Li T. Post-COVID-19 longitudinally extensive transverse myelitis with myelin oligodendrocyte glycoprotein antibodies. Case Rep Neurol Med 2022; 2022: 1068227
    PubMedGoogle Scholar
  • 33 Doukas SG, Santos AP, Mir W, Daud S, Zivin-Tutela TH. A rare case of myelin oligodendrocyte glycoprotein antibody-associated transverse myelitis in a 40-year-old patient with COVID-19. Cureus 2022; 14 (04) e23877
    PubMedGoogle Scholar
  • 34 Peters J, Alhasan S, Vogels CBF, Grubaugh ND, Farhadian S, Longbrake EE. MOG-associated encephalitis following SARS-COV-2 infection. Mult Scler Relat Disord 2021; 50: 102857
    CrossrefPubMedGoogle Scholar
  • 35 Durovic E, Bien C, Bien CG, Isenmann S. MOG antibody-associated encephalitis secondary to COVID-19: case report. BMC Neurol 2021; 21 (01) 414
    CrossrefPubMedGoogle Scholar
  • 36 Vraka K, Ram D, West S. et al. Two paediatric patients with encephalopathy and concurrent COVID-19 infection: two sides of the same coin?. Case Rep Neurol Med 2021; 2021: 6658000
    PubMedGoogle Scholar
  • 37 Jossy A, Jacob N, Sarkar S, Gokhale T, Kaliaperumal S, Deb AK. COVID-19-associated optic neuritis - a case series and review of literature. Indian J Ophthalmol 2022; 70 (01) 310-316
    CrossrefPubMedGoogle Scholar
  • 38 Ide T, Kawanami T, Eriguchi M, Hara H. SARS-CoV-2-related myelin oligodendrocyte glycoprotein antibody-associated disease: a case report and literature review. Intern Med 2022; 61 (08) 1253-1258
    CrossrefPubMedGoogle Scholar
  • 39 Balasa A, Neely B, McGuire S. A case of a 14 year old male with MOGAD (myelin oligocyte glycoprotein antibody disease) post-COVID-19 infection responsive to high dose corticosteroids and intravenous immunoglobulin (IVIG) therapy. Neurology 2022
    PubMedGoogle Scholar
  • 40 Pinto AA, Carroll LS, Nar V, Varatharaj A, Galea I. CNS inflammatory vasculopathy with antimyelin oligodendrocyte glycoprotein antibodies in COVID-19. Neurol Neuroimmunol Neuroinflamm 2020; 7 (05) e813
    CrossrefPubMedGoogle Scholar
  • 41 Žorić L, Rajović-Mrkić I, Čolak E, Mirić D, Kisić B. Optic neuritis in a patient with seropositive myelin oligodendrocyte glycoprotein antibody during the post-COVID-19 period. Int Med Case Rep J 2021; 14: 349-355
    CrossrefPubMedGoogle Scholar
  • 42 Wynford-Thomas R, Jacob A, Tomassini V. Neurological update: MOG antibody disease. J Neurol 2019; 266 (05) 1280-1286
    CrossrefPubMedGoogle Scholar
  • 43 Pace S, Orrell M, Woodhall M. et al. Frequency of MOG-IgG in cerebrospinal fluid versus serum. J Neurol Neurosurg Psychiatry 2022; 93 (03) 334-335
    CrossrefPubMedGoogle Scholar
  • 44 Assavapongpaiboon B, Apinyawasisuk S, Jariyakosol S. Myelin oligodendrocyte glycoprotein antibody-associated optic neuritis with COVID-19 infection: a case report and literature review. Am J Ophthalmol Case Rep 2022; 26: 101491
    CrossrefPubMedGoogle Scholar
  • 45 López-Chiriboga AS, Majed M, Fryer J. et al. Association of MOG-IgG serostatus with relapse after acute disseminated encephalomyelitis and proposed diagnostic criteria for MOG-IgG-associated disorders. JAMA Neurol 2018; 75 (11) 1355-1363
    CrossrefPubMedGoogle Scholar
  • 46 Marignier R, Hacohen Y, Cobo-Calvo A. et al. Myelin-oligodendrocyte glycoprotein antibody-associated disease. Lancet Neurol 2021; 20 (09) 762-772
    CrossrefPubMedGoogle Scholar
  • 47 Wingerchuk DM, Banwell B, Bennett JL. et al; International Panel for NMO Diagnosis. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology 2015; 85 (02) 177-189
    CrossrefPubMedGoogle Scholar
  • 48 Mirmosayyeb O, Ghaffary EM, Bagherieh S, Barzegar M, Dehghan MS, Shaygannejad V. Post COVID-19 infection neuromyelitis optica spectrum disorder (NMOSD): a case report-based systematic review. Mult Scler Relat Disord 2022; 60: 103697
    CrossrefPubMedGoogle Scholar
  • 49 Batum M, Kisabay Ak A, Mavioğlu H. COVID-19 infection-induced neuromyelitis optica: a case report. Int J Neurosci 2022; 132 (10) 999-1004
    CrossrefPubMedGoogle Scholar
  • 50 Jentzer A, Carra-Dallière C, Lozano C. et al. Neuromyelitis optica spectrum disorder following COVID-19 infection with increase in pre-existing anti-aquaporin-4 antibodies. J Neurol 2022; 269 (06) 2850-2853
    CrossrefPubMedGoogle Scholar
  • 51 Ghosh R, De K, Roy D. et al. A case of area postrema variant of neuromyelitis optica spectrum disorder following SARS-CoV-2 infection. J Neuroimmunol 2020; 350: 577439
    CrossrefPubMedGoogle Scholar
  • 52 Shaw VC, Chander G, Puttanna A. Neuromyelitis optica spectrum disorder secondary to COVID-19. Br J Hosp Med (Lond) 2020; 81 (09) 1-3
    CrossrefPubMedGoogle Scholar
  • 53 Chuang T-Y, Miskin D. Case report: neuromyelitis optica associated with SARS-CoV-2. Pract Neurol 2020
    PubMedGoogle Scholar
  • 54 Zoghi A, Ramezani M, Roozbeh M, Darazam IA, Sahraian MA. A case of possible atypical demyelinating event of the central nervous system following COVID-19. Mult Scler Relat Disord 2020; 44: 102324
    CrossrefPubMedGoogle Scholar
  • 55 Rafique S, Wasim A, Sultan T, Ahmad A. Post-COVID neuromyelitis optica spectrum disorder. J Coll Physicians Surg Pak 2021; 31 (07) 138-140
    PubMedGoogle Scholar
  • 56 Das D, Bhattacharjee H, Rehman O. et al. Neuromyelitis optica spectrum disorder post-COVID-19 infection: a rare case report from Northeast India. Indian J Ophthalmol 2022; 70 (05) 1833-1836
    CrossrefPubMedGoogle Scholar
  • 57 Kovalev D, Thottempudi N, Ahmed A, Shanina E. New-onset neuromyelitis optica spectrum disorder in a patient with COVID-19 and chronic hepatitis B co-infection. Neuroimmunology Reports 2022; 2: 100063
    CrossrefPubMedGoogle Scholar
  • 58 Barone S, Rapisarda L, Manzo L. et al. A case of neuromyelitis optica spectrum disorder (NMOSD) and acute myositis following SARS-CoV-2 infection. J Neurol Sci 2021; 429 DOI: 10.1016/j.jns.2021.119862.
    CrossrefPubMedGoogle Scholar
  • 59 Holroyd KB, Manzano GS, Levy M. Update on neuromyelitis optica spectrum disorder. Curr Opin Ophthalmol 2020; 31 (06) 462-468
    CrossrefPubMedGoogle Scholar
  • 60 Schulte EC, Hauer L, Kunz AB, Sellner J. Systematic review of cases of acute myelitis in individuals with COVID-19. Eur J Neurol 2021; 28 (10) 3230-3244
    CrossrefPubMedGoogle Scholar
  • 61 Ahmad SA, Salih KH, Ahmed SF. et al. Post COVID-19 transverse myelitis; a case report with review of literature. Ann Med Surg (Lond) 2021; 69: 102749
    PubMedGoogle Scholar
  • 62 Zanin L, Saraceno G, Panciani PP. et al. SARS-CoV-2 can induce brain and spine demyelinating lesions. Acta Neurochir (Wien) 2020; 162 (07) 1491-1494
    CrossrefPubMedGoogle Scholar
  • 63 Rossi T, Novi G, D'Agostino I. et al. Bilateral optic neuritis as the presenting sign of post SARS-CoV-2 acute disseminated encephalomyelitis. Am J Ophthalmol Case Rep 2022; 25: 101273
    CrossrefPubMedGoogle Scholar
  • 64 Gelibter S, Bellavia G, Arbasino C. et al. Encephalopathy as a prognostic factor in adults with acute disseminated encephalomyelitis following COVID-19. J Neurol 2022; 269 (05) 2293-2300
    CrossrefPubMedGoogle Scholar
  • 65 Oumerzouk J, Nabil M, Klevor R. et al. Clinicoradiological and prognostic features of COVID-19-associated acute disseminated encephalomyelitis. Rev Neurol (Paris) 2022; 178 (1-2): 144-150
    CrossrefPubMedGoogle Scholar
  • 66 Valencia Sanchez C, Theel E, Binnicker M, Toledano M, McKeon A. Autoimmune encephalitis after SARS-CoV-2 infection: case frequency, findings, and outcomes. Neurology 2021; 97 (23) e2262-e2268
    CrossrefPubMedGoogle Scholar
  • 67 Nabizadeh F, Balabandian M, Sodeifian F, Rezaei N, Rostami MR, Naser Moghadasi A. Autoimmune encephalitis associated with COVID-19: a systematic review. Mult Scler Relat Disord 2022; 62: 103795
    CrossrefPubMedGoogle Scholar
  • 68 Payus AO, Jeffree MS, Ohn MH. et al. Immune-mediated neurological syndrome in SARS-CoV-2 infection: a review of literature on autoimmune encephalitis in COVID-19. Neurol Sci 2022; 43 (03) 1533-1547
    CrossrefPubMedGoogle Scholar
  • 69 Stoian A, Stoian M, Bajko Z. et al. Autoimmune encephalitis in COVID-19 infection: our experience and systematic review of the literature. Biomedicines 2022; 10 (04) 774
    CrossrefPubMedGoogle Scholar
  • 70 Grimaldi S, Lagarde S, Harlé JR, Boucraut J, Guedj E. Autoimmune encephalitis concomitant with SARS-CoV-2 infection: insight from 18F-FDG PET imaging and neuronal autoantibodies. J Nucl Med 2020; 61 (12) 1726-1729
    CrossrefPubMedGoogle Scholar
  • 71 Bodro M, Compta Y, Llansó L. et al; “Hospital Clínic Infecto-COVID-19” and “Hospital Clínic Neuro-COVID-19” Groups. Increased CSF levels of IL-1β, IL-6, and ACE in SARS-CoV-2-associated encephalitis. Neurol Neuroimmunol Neuroinflamm 2020; 7 (05) e821
    CrossrefPubMedGoogle Scholar
  • 72 Graus F, Titulaer MJ, Balu R. et al. A clinical approach to diagnosis of autoimmune encephalitis. Lancet Neurol 2016; 15 (04) 391-404
    CrossrefPubMedGoogle Scholar
  • 73 Keller E, Brandi G, Winklhofer S. et al. Large and small cerebral vessel involvement in severe COVID-19: detailed clinical workup of a case series. Stroke 2020; 51 (12) 3719-3722
    CrossrefPubMedGoogle Scholar
  • 74 Lersy F, Anheim M, Willaume T. et al. Cerebral vasculitis of medium-sized vessels as a possible mechanism of brain damage in COVID-19 patients. J Neuroradiol 2021; 48 (03) 141-146
    CrossrefPubMedGoogle Scholar
  • 75 Timmons GM, Rempe T, Bevins EA. et al. CNS lymphocytic vasculitis in a young woman with COVID-19 infection. Neurol Neuroimmunol Neuroinflamm 2021; 8 (05) e1048
    CrossrefPubMedGoogle Scholar
  • 76 Dixon L, Coughlan C, Karunaratne K. et al. Immunosuppression for intracranial vasculitis associated with SARS-CoV-2: therapeutic implications for COVID-19 cerebrovascular pathology. J Neurol Neurosurg Psychiatry 2020; jnnp-2020-324291
    PubMedGoogle Scholar
  • 77 Oliveira RMC, Santos DH, Olivetti BC, Takahashi JT. Bilateral trochlear nerve palsy due to cerebral vasculitis related to COVID-19 infection. Arq Neuropsiquiatr 2020; 78 (06) 385-386
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 78 Vaschetto R, Cena T, Sainaghi PP. et al. Cerebral nervous system vasculitis in a COVID-19 patient with pneumonia. J Clin Neurosci 2020; 79: 71-73
    CrossrefPubMedGoogle Scholar
  • 79 Hanafi R, Roger PA, Perin B. et al. COVID-19 neurologic complication with CNS vasculitis-like pattern. AJNR Am J Neuroradiol 2020; 41 (08) 1384-1387
    CrossrefPubMedGoogle Scholar
  • 80 Nannoni S, de Groot R, Bell S, Markus HS. Stroke in COVID-19: a systematic review and meta-analysis. Int J Stroke 2021; 16 (02) 137-149
    CrossrefPubMedGoogle Scholar
  • 81 Bhattacharyya S, Berkowitz AL. Primary angiitis of the central nervous system: avoiding misdiagnosis and missed diagnosis of a rare disease. Pract Neurol 2016; 16 (03) 195-200
    CrossrefPubMedGoogle Scholar
  • 82 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 (09) 1079-1088
    CrossrefPubMedGoogle Scholar
  • 83 Salter A, Fox RJ, Newsome SD. et al. Outcomes and risk factors associated with SARS-CoV-2 infection in a North American Registry of patients with multiple sclerosis. JAMA Neurol 2021; 78 (06) 699-708
    CrossrefPubMedGoogle Scholar
  • 84 Finsterer J. SARS-CoV-2 triggered relapse of multiple sclerosis. Clin Neurol Neurosurg 2022; 215: 107210
    CrossrefPubMedGoogle Scholar
  • 85 Etemadifar M, Abhari AP, Nouri H. et al. Does COVID-19 increase the long-term relapsing-remitting multiple sclerosis clinical activity? A cohort study. BMC Neurol 2022; 22 (01) 64
    CrossrefPubMedGoogle Scholar
  • 86 Etemadifar M, Sedaghat N, Aghababaee A. et al. COVID-19 and the risk of relapse in multiple sclerosis patients: a fight with no bystander effect?. Mult Scler Relat Disord 2021; 51: 102915
    CrossrefPubMedGoogle Scholar
  • 87 Barzegar M, Vaheb S, Mirmosayyeb O, Afshari-Safavi A, Nehzat N, Shaygannejad V. Can coronavirus disease 2019 (COVID-19) trigger exacerbation of multiple sclerosis? A retrospective study. Mult Scler Relat Disord 2021; 52: 102947
    CrossrefPubMedGoogle Scholar
  • 88 Garjani A, Middleton RM, Nicholas R, Evangelou N. Recovery from COVID-19 in multiple sclerosis: a prospective and longitudinal cohort study of the United Kingdom multiple sclerosis register. Neurol Neuroimmunol Neuroinflamm 2021; 9 (01) e1118
    CrossrefPubMedGoogle Scholar
  • 89 Czarnowska A, Kapica-Topczewska K, Zajkowska O. et al. Symptoms after COVID-19 infection in individuals with multiple sclerosis in Poland. J Clin Med 2021; 10 (22) 5225
    CrossrefPubMedGoogle Scholar
  • 90 Newsome SD, Cross AH, Fox RJ. et al. COVID-19 in patients with neuromyelitis optica spectrum disorders and myelin oligodendrocyte glycoprotein antibody disease in North America: from the COViMS Registry. Neurol Neuroimmunol Neuroinflamm 2021; 8 (05) e1057
    CrossrefPubMedGoogle Scholar
  • 91 Sen S, Tuncer A, Ozakbas S. et al. The Turkish experience of COVID-19 infection in people with NMOSD and MOGAD: a milder course?. Mult Scler Relat Disord 2022; 58: 103399
    CrossrefPubMedGoogle Scholar
  • 92 Woodhall M, Mitchell JW, Gibbons E, Healy S, Waters P, Huda S. Case report: myelin oligodendrocyte glycoprotein antibody-associated relapse with COVID-19. Front Neurol 2020; 11: 598531
    CrossrefPubMedGoogle Scholar
  • 93 Barzegar M, Mirmosayyeb O, Ebrahimi N. et al. COVID-19 susceptibility and outcomes among patients with neuromyelitis optica spectrum disorder (NMOSD): a systematic review and meta-analysis. Mult Scler Relat Disord 2022; 57: 103359
    CrossrefPubMedGoogle Scholar
  • 94 Alonso R, Silva B, Garcea O. et al. COVID-19 in multiple sclerosis and neuromyelitis optica spectrum disorder patients in Latin America: COVID-19 in MS and NMOSD patients in LATAM. Mult Scler Relat Disord 2021; 51: 102886
    CrossrefPubMedGoogle Scholar
  • 95 Apostolos-Pereira SL, Campos Ferreira L, Boaventura M. et al; Neuroimmunology Brazilian Study Group. Clinical features of COVID-19 on patients with neuromyelitis optica spectrum disorders. Neurol Neuroimmunol Neuroinflamm 2021; 8 (06) e1060
    CrossrefPubMedGoogle Scholar
  • 96 Moreno-Torres V, Mendoza C, Mellor-Pita S. et al. Systemic autoimmune diseases in patients hospitalized with COVID-19 in Spain: a nation-wide registry study. Viruses 2022; 14 (08) 1631
    CrossrefPubMedGoogle Scholar
  • 97 Mehta P, Gasparyan AY, Zimba O, Kitas GD. Systemic lupus erythematosus in the light of the COVID-19 pandemic: infection, vaccination, and impact on disease management. Clin Rheumatol 2022; 41 (09) 2893-2910
    CrossrefPubMedGoogle Scholar
  • 98 Lotan I, Wilf-Yarkoni A, Friedman Y, Stiebel-Kalish H, Steiner I, Hellmann MA. Safety of the BNT162b2 COVID-19 vaccine in multiple sclerosis (MS): early experience from a tertiary MS center in Israel. Eur J Neurol 2021; 28 (11) 3742-3748
    CrossrefPubMedGoogle Scholar
  • 99 Ciampi E, Uribe-San-Martin R, Soler B. et al. Safety and humoral response rate of inactivated and mRNA vaccines against SARS-CoV-2 in patients with multiple sclerosis. Mult Scler Relat Disord 2022; 59: 103690
    CrossrefPubMedGoogle Scholar
  • 100 Baden LR, El Sahly HM, Essink B. et al; COVE Study Group. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med 2021; 384 (05) 403-416
    CrossrefPubMedGoogle Scholar
  • 101 Polack FP, Thomas SJ, Kitchin N. et al; C4591001 Clinical Trial Group. Safety and efficacy of the BNT162b2 mRNA COVID-19 vaccine. N Engl J Med 2020; 383 (27) 2603-2615
    CrossrefPubMedGoogle Scholar
  • 102 Katz JD, Bouley AJ, Jungquist RM, Douglas EA, O'Shea IL, Lathi ES. Humoral and T-cell responses to SARS-CoV-2 vaccination in multiple sclerosis patients treated with ocrelizumab. Mult Scler Relat Disord 2022; 57: 103382
    CrossrefPubMedGoogle Scholar
  • 103 Novak F, Nilsson AC, Nielsen C. et al. Humoral immune response following SARS-CoV-2 mRNA vaccination concomitant to anti-CD20 therapy in multiple sclerosis. Mult Scler Relat Disord 2021; 56: 103251
    CrossrefPubMedGoogle Scholar
  • 104 Achiron A, Mandel M, Dreyer-Alster S. et al. Humoral immune response to COVID-19 mRNA vaccine in patients with multiple sclerosis treated with high-efficacy disease-modifying therapies. Ther Adv Neurol Disord 2021; 14: 17 562864211012835
    CrossrefPubMedGoogle Scholar
  • 105 Dreyer-Alster S, Menascu S, Mandel M. et al. COVID-19 vaccination in patients with multiple sclerosis: safety and humoral efficacy of the third booster dose. J Neurol Sci 2022; 434: 120155
    CrossrefPubMedGoogle Scholar
  • 106 Palomares Cabeza V, Kummer LYL, Wieske L. et al; Target-to-B! (T2B!) SARS-CoV-2 Study Group. Longitudinal T-cell responses after a third SARS-CoV-2 vaccination in patients with multiple sclerosis on ocrelizumab or fingolimod. Neurol Neuroimmunol Neuroinflamm 2022; 9 (04) e1178
    CrossrefPubMedGoogle Scholar
  • 107 Achiron A, Mandel M, Dreyer-Alster S. et al. Humoral immune response in multiple sclerosis patients following PfizerBNT162b2 COVID19 vaccination: up to 6 months cross-sectional study. J Neuroimmunol 2021; 361: 577746
    CrossrefPubMedGoogle Scholar
  • 108 Furer V, Eviatar T, Zisman D. et al. Immunogenicity and safety of the BNT162b2 mRNA COVID-19 vaccine in adult patients with autoimmune inflammatory rheumatic diseases and in the general population: a multicentre study. Ann Rheum Dis 2021; 80 (10) 1330-1338
    CrossrefPubMedGoogle Scholar
  • 109 Lotan I, Romanow G, Levy M. Patient-reported safety and tolerability of the COVID-19 vaccines in persons with rare neuroimmunological diseases. Mult Scler Relat Disord 2021; 55: 103189
    CrossrefPubMedGoogle Scholar
  • 110 Maarouf A, Rico A, Boutiere C. et al; Under the Aegis of OFSEP. Extending rituximab dosing intervals in patients with MS during the COVID-19 pandemic and beyond?. Neurol Neuroimmunol Neuroinflamm 2020; 7 (05) e825
    CrossrefPubMedGoogle Scholar
  • 111 Nielsen AS, Miravalle A, Langer-Gould A, Cooper J, Edwards KR, Kinkel RP. Maximally tolerated versus minimally effective dose: the case of rituximab in multiple sclerosis. Mult Scler 2012; 18 (03) 377-378
    CrossrefPubMedGoogle Scholar
  • 112 Yang CS, Yang L, Li T. et al. Responsiveness to reduced dosage of rituximab in Chinese patients with neuromyelitis optica. Neurology 2013; 81 (08) 710-713
    CrossrefPubMedGoogle Scholar
  • 113 Lebrun C, Cohen M, Rosenthal-Allieri MA. et al. Only follow-up of memory B cells helps monitor rituximab administration to patients with neuromyelitis optica spectrum disorders. Neurol Ther 2018; 7 (02) 373-383
    CrossrefPubMedGoogle Scholar
  • 114 Tolf A, Wiberg A, Müller M. et al. Factors associated with serological response to SARS-CoV-2 vaccination in patients with multiple sclerosis treated with rituximab. JAMA Netw Open 2022; 5 (05) e2211497
    CrossrefPubMedGoogle Scholar
  • 115 Asplund Högelin K, Ruffin N, Pin E. et al. B-cell repopulation dynamics and drug pharmacokinetics impact SARS-CoV-2 vaccine efficacy in anti-CD20-treated multiple sclerosis patients. Eur J Neurol 2022; 29 (11) 3317-3328
    CrossrefPubMedGoogle Scholar
  • 116 Hammond J, Leister-Tebbe H, Gardner A. et al; EPIC-HR Investigators. Oral nirmatrelvir for high-risk, nonhospitalized adults with COVID-19. N Engl J Med 2022; 386 (15) 1397-1408
    CrossrefPubMedGoogle Scholar
  • 117 Coulson JM, Adams A, Gray LA, Evans A. COVID-19 “Rebound” associated with nirmatrelvir/ritonavir pre-hospital therapy. J Infect 2022; 85 (04) 436-480
    CrossrefPubMedGoogle Scholar
  • 118 Fact Sheet for Healthcare Providers: Emergency Use Authorization for Paxlovid. Available at: https://www.fda.gov/media/155050/download
    PubMed
  • 119 Manzano GS, Rice DR, Klawiter EC. et al. Anti-SARS-CoV-2 monoclonal antibodies for the treatment of active COVID-19 in multiple sclerosis: an observational study. Mult Scler 2022; 28 (07) 1146-1150
    CrossrefPubMedGoogle Scholar
  • 120 Levin MJ, Ustianowski A, De Wit S. et al; PROVENT Study Group. Intramuscular AZD7442 (Tixagevimab-Cilgavimab) for prevention of COVID-19. N Engl J Med 2022; 386 (23) 2188-2200
    CrossrefPubMedGoogle Scholar
  • 121 Fact Sheet for Healthcare Providers: Emergency Use Authorization for Evusheld. Available at: https://www.fda.gov/media/154701/download
    PubMed
  • 122 Al Jurdi A, Morena L, Cote M, Bethea E, Azzi J, Riella LV. Tixagevimab/cilgavimab pre-exposure prophylaxis is associated with lower breakthrough infection risk in vaccinated solid organ transplant recipients during the omicron wave. Am J Transplant 2022; 22 (12) 3130-3136
    CrossrefPubMedGoogle Scholar
  • 123 Conte WL, Golzarri-Arroyo L. Tixagevimab and cilgavimab (Evusheld) boosts antibody levels to SARS-CoV-2 in patients with multiple sclerosis on b-cell depleters. Mult Scler Relat Disord 2022; 63: 103905
    CrossrefPubMedGoogle Scholar
  • 124 Alwan NA, Johnson L. Defining long COVID: going back to the start. Med (N Y) 2021; 2 (05) 501-504
    CrossrefPubMedGoogle Scholar
  • 125 Datta SD, Talwar A, Lee JT. A proposed framework and timeline of the spectrum of disease due to SARS-CoV-2 infection: illness beyond acute infection and public health implications. JAMA 2020; 324 (22) 2251-2252
    CrossrefPubMedGoogle Scholar
  • 126 Garjani A, Middleton RM, Hunter R. et al. COVID-19 is associated with new symptoms of multiple sclerosis that are prevented by disease modifying therapies. Mult Scler Relat Disord 2021; 52: 102939
    CrossrefPubMedGoogle Scholar
  • 127 Fragoso YD, Pacheco FAS, Silveira GL, Oliveira RA, Carvalho VM, Martimbianco ALC. COVID-19 in a temporal relation to the onset of multiple sclerosis. Mult Scler Relat Disord 2021; 50: 102863
    CrossrefPubMedGoogle Scholar
  • 128 Domingues RB, Mendes-Correa MC, de Moura Leite FBV. et al. First case of SARS-COV-2 sequencing in cerebrospinal fluid of a patient with suspected demyelinating disease. J Neurol 2020; 267 (11) 3154-3156
    CrossrefPubMedGoogle Scholar
  • 129 Sardar S, Safan A, Okar L, Sadik N, Adeli G. The diagnostic dilemma of bilateral optic neuritis and idiopathic intracranial hypertension coexistence in a patient with recent COVID-19 infection. Clin Case Rep 2021; 9 (06) e04347
    CrossrefPubMedGoogle Scholar
  • 130 Simpson-Yap S, De Brouwer E, Kalincik T. et al. Associations of disease-modifying therapies with COVID-19 severity in multiple sclerosis. Neurology 2021; 97 (19) e1870-e1885
    CrossrefPubMedGoogle Scholar
  • 131 Gombolay GY, Dutt M, Tyor W. Immune responses to SARS-CoV-2 vaccination in multiple sclerosis: a systematic review/meta-analysis. Ann Clin Transl Neurol 2022; 9 (08) 1321-1331
    CrossrefPubMedGoogle Scholar
  • 132 Freedman MS, Jack D, Murgašová Z, Todorović M, Seitzinger A. Outcomes of COVID-19 among patients treated with subcutaneous interferon beta-1a for multiple sclerosis. Mult Scler Relat Disord 2021; 56: 103283
    CrossrefPubMedGoogle Scholar
  • 133 Simpson-Yap S, Pirmani A, De Brouwer E. et al. Severity of COVID19 infection among patients with multiple sclerosis treated with interferon-β. Mult Scler Relat Disord 2022; 66: 104072
    CrossrefPubMedGoogle Scholar
  • 134 Milo R, Staun-Ram E, Karussis D. et al; Israeli Neuroimmunology Study Group on COVID-19 Vaccination in Multiple Sclerosis. Humoral and cellular immune responses to SARS-CoV-2 mRNA vaccination in patients with multiple sclerosis: an Israeli multi-center experience following 3 vaccine doses. Front Immunol 2022; 13: 868915
    CrossrefPubMedGoogle Scholar
  • 135 Kister I, Patskovsky Y, Curtin R. et al. Cellular and humoral immunity to SARS-CoV-2 infection in multiple sclerosis patients on ocrelizumab and other disease-modifying therapies: a multi-ethnic observational study. Ann Neurol 2022; 91 (06) 782-795
    CrossrefPubMedGoogle Scholar
  • 136 Tortorella C, Aiello A, Gasperini C. et al; INMI COVID-19 Vaccine Study Group. Humoral- and T-cell-specific immune responses to SARS-CoV-2 mRNA vaccination in patients with MS using different disease-modifying therapies. Neurology 2022; 98 (05) e541-e554
    CrossrefPubMedGoogle Scholar
  • 137 Sullivan R, Kilaru A, Hemmer B. et al. COVID-19 infection in fingolimod- or siponimod-treated patients: case series. Neurol Neuroimmunol Neuroinflamm 2021; 9 (01) e1092
    CrossrefPubMedGoogle Scholar
  • 138 Cross AH, Delgado S, Habek M. et al. COVID-19 outcomes and vaccination in people with relapsing multiple sclerosis treated with ofatumumab. Neurol Ther 2022; 11 (02) 741-758
    CrossrefPubMedGoogle Scholar
  • 139 Mimori M, Komatsu T, Maku T, Mitsumura H, Iguchi Y. Generalized myasthenia gravis patients infected with COVID-19 should continue eculizumab. Neurol Sci 2022; 43 (07) 4081-4083
    CrossrefPubMedGoogle Scholar
  • 140 Fodil S, Annane D. Complement inhibition and COVID-19: the story so far. ImmunoTargets Ther 2021; 10: 273-284
    CrossrefPubMedGoogle Scholar
  • 141 Jovicevic V, Ivanovic J, Momcilovic N. et al. Humoral response to SARS-CoV-2 infection and vaccines against COVID-19 in patients with neuromyelitis optica spectrum disorders: impact of immunosuppressive treatment. Mult Scler Relat Disord 2022; 62: 103794
    CrossrefPubMedGoogle Scholar
  • 142 Svačina MKR, Meißner A, Schweitzer F. et al. Antibody response after COVID-19 vaccination in intravenous immunoglobulin-treated immune neuropathies. Eur J Neurol 2022; 29 (11) 3380-3388
    CrossrefPubMedGoogle Scholar
  • 143 Ugarte-Gil MF, Alarcón GS, Izadi Z. et al. Characteristics associated with poor COVID-19 outcomes in individuals with systemic lupus erythematosus: data from the COVID-19 Global Rheumatology Alliance. Ann Rheum Dis 2022; 81 (07) 970-978
    CrossrefPubMedGoogle Scholar
  • 144 Meshram HS, Kute V, Rane H. et al. Humoral and cellular response of COVID-19 vaccine among solid organ transplant recipients: a systematic review and meta-analysis. Transpl Infect Dis 2022; 24 (06) e13926
    CrossrefPubMedGoogle Scholar
  • 145 De Santis M, Motta F, Isailovic N. et al. Dose-dependent impairment of the immune response to the Moderna-1273 mRNA vaccine by mycophenolate mofetil in patients with rheumatic and autoimmune liver diseases. Vaccines (Basel) 2022; 10 (05) 801
    CrossrefPubMedGoogle Scholar
  • 146 Krasselt M, Wagner U, Nguyen P. et al. Humoral and cellular response to COVID-19 vaccination in patients with autoimmune inflammatory rheumatic diseases under real-life conditions. Rheumatology (Oxford) 2022; 61 (SI2): SI180-SI188
    CrossrefPubMedGoogle Scholar
  • 147 Kashiwado Y, Kimoto Y, Sawabe T. et al. Antibody response to SARS-CoV-2 mRNA vaccines in patients with rheumatic diseases in Japan: interim analysis of a multicenter cohort study. Mod Rheumatol 2022; roac030
    PubMedGoogle Scholar
  • 148 Izadi Z, Brenner EJ, Mahil SK. et al; Psoriasis Patient Registry for Outcomes, Therapy and Epidemiology of COVID-19 Infection (PsoProtect); the Secure Epidemiology of Coronavirus Under Research Exclusion for Inflammatory Bowel Disease (SECURE-IBD); and the COVID-19 Global Rheumatology Allianc, Psoriasis Patient Registry for Outcomes, Therapy and Epidemiology of COVID-19 Infection (PsoProtect); the Secure Epidemiology of Coronavirus Under Research Exclusion for Inflammatory Bowel Disease (SECURE-IBD); and the COVID-19 Global Rheumatology Alliance (GRA). Association between tumor necrosis factor inhibitors and the risk of hospitalization or death among patients with immune-mediated inflammatory disease and COVID-19. JAMA Netw Open 2021; 4 (10) e2129639
    CrossrefPubMedGoogle Scholar
  • 149 Monti S, Fornara C, Delvino P. et al. Immunosuppressive treatments selectively affect the humoral and cellular response to SARS-CoV-2 in vaccinated patients with vasculitis. Rheumatology (Oxford) 2023; 62 (02) 726-734
    CrossrefPubMedGoogle Scholar
  • 150 Haberman RH, Herati R, Simon D. et al. Methotrexate hampers immunogenicity to BNT162b2 mRNA COVID-19 vaccine in immune-mediated inflammatory disease. Ann Rheum Dis 2021; 80 (10) 1339-1344
    CrossrefPubMedGoogle Scholar
  • 151 Mahil SK, Bechman K, Raharja A. et al. Humoral and cellular immunogenicity to a second dose of COVID-19 vaccine BNT162b2 in people receiving methotrexate or targeted immunosuppression: a longitudinal cohort study. Lancet Rheumatol 2022; 4 (01) e42-e52
    CrossrefPubMedGoogle Scholar
  • 152 Abhishek A, Boyton RJ, Peckham N. et al; VROOM Study Investigators. Effect of a 2-week interruption in methotrexate treatment versus continued treatment on COVID-19 booster vaccine immunity in adults with inflammatory conditions (VROOM study): a randomised, open label, superiority trial. Lancet Respir Med 2022; 10 (09) 840-850
    CrossrefPubMedGoogle Scholar
  • 153 Kennedy NA, Lin S, Goodhand JR. et al; Contributors to the CLARITY IBD Study. Infliximab is associated with attenuated immunogenicity to BNT162b2 and ChAdOx1 nCoV-19 SARS-CoV-2 vaccines in patients with IBD. Gut 2021; 70 (10) 1884-1893
    CrossrefPubMedGoogle Scholar
  • 154 Vollenberg R, Tepasse PR, Lorentzen E, Nowacki TM. Impaired humoral immunity with concomitant preserved T cell reactivity in IBD patients on treatment with infliximab 6 month after vaccination with the SARS-CoV-2 mRNA vaccine BNT162b2: a pilot study. J Pers Med 2022; 12 (05) 694
    CrossrefPubMedGoogle Scholar
  • 155 Bar-Or A, Wiendl H, Miller B. et al. Randomized study of teriflunomide effects on immune responses to neoantigen and recall antigens. Neurol Neuroimmunol Neuroinflamm 2015; 2 (02) e70
    CrossrefPubMedGoogle Scholar
  • 156 Rutgers A, Westerweel PE, van der Holt B. et al. Timely administration of tocilizumab improves outcome of hospitalized COVID-19 patients. PLoS One 2022; 17 (08) e0271807
    CrossrefPubMedGoogle Scholar