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Neuromyelitis Optica Spectrum Disorders

  • Massimo Filippi
  • Maria A. Rocca
Chapter
  • 37 Downloads

Abstract

Neuromyelitis optica spectrum disorders (NMOSD) are a heterogeneous group of inflammatory, demyelinating and antibody-mediated diseases of the central nervous system (CNS). The anti-aquaporin-4-IgG (AQP4-IgG) seems to be the pathogenetic agent, being present in the large majority of patients, although seronegative forms can occur. Clinical manifestations include core features, such as myelitis, optic neuritis, and area postrema syndrome, possibly associated with collateral symptoms like pain, dystonic movements, and pruritus. Diagnosis is based on both clinical presentation and anti-AQP4-IgG testing. MRI features provide supportive elements in seronegative patients. The most effective therapy in acute attacks is plasma exchange, whereas multiple drugs are used for chronic maintenance (azathioprine, mycophenolate mofetil, rituximab and eculizumab).

References

  1. 1.
    Waters P, Reindl M, Saiz A, Schanda K, Tuller F, Kral V, et al. Multicentre comparison of a diagnostic assay: aquaporin-4 antibodies in neuromyelitis optica. J Neurol Neurosurg Psychiatry. 2016;87(9):1005–15.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology. 2015;85(2):177–89.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Flanagan EP, Cabre P, Weinshenker BG, Sauver JS, Jacobson DJ, Majed M, et al. Epidemiology of aquaporin-4 autoimmunity and neuromyelitis optica spectrum. Ann Neurol. 2016;79(5):775–83.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bukhari W, Prain KM, Waters P, Woodhall M, O’Gorman CM, Clarke L, et al. Incidence and prevalence of NMOSD in Australia and New Zealand. J Neurol Neurosurg Psychiatry. 2017;88(8):632–8.CrossRefGoogle Scholar
  5. 5.
    Etemadifar M, Nasr Z, Khalili B, Taherioun M, Vosoughi R. Epidemiology of neuromyelitis optica in the world: a systematic review and meta-analysis. Mult Scler Int. 2015;2015:174720.PubMedPubMedCentralGoogle Scholar
  6. 6.
    Etemadifar M, Dashti M, Vosoughi R, Abtahi SH, Ramagopalan SV, Nasr Z. An epidemiological study of neuromyelitis optica in Isfahan. Mult Scler. 2014;20(14):1920–2.CrossRefGoogle Scholar
  7. 7.
    Jacob A, Panicker J, Lythgoe D, Elsone L, Mutch K, Wilson M, et al. The epidemiology of neuromyelitis optica amongst adults in the Merseyside county of United Kingdom. J Neurol. 2013;260(8):2134–7.CrossRefGoogle Scholar
  8. 8.
    Cabrera-Gomez JA, Kurtzke JF, Gonzalez-Quevedo A, Lara-Rodriguez R. An epidemiological study of neuromyelitis optica in Cuba. J Neurol. 2009;256(1):35–44.CrossRefGoogle Scholar
  9. 9.
    Houzen H, Niino M, Hirotani M, Fukazawa T, Kikuchi S, Tanaka K, et al. Increased prevalence, incidence, and female predominance of multiple sclerosis in northern Japan. J Neurol Sci. 2012;323(1–2):117–22.CrossRefGoogle Scholar
  10. 10.
    Asgari N, Lillevang ST, Skejoe HP, Falah M, Stenager E, Kyvik KO. A population-based study of neuromyelitis optica in Caucasians. Neurology. 2011;76(18):1589–95.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Cossburn M, Tackley G, Baker K, Ingram G, Burtonwood M, Malik G, et al. The prevalence of neuromyelitis optica in south East Wales. Eur J Neurol. 2012;19(4):655–9.CrossRefGoogle Scholar
  12. 12.
    Aboul-Enein F, Seifert-Held T, Mader S, Kuenz B, Lutterotti A, Rauschka H, et al. Neuromyelitis optica in Austria in 2011: to bridge the gap between neuroepidemiological research and practice in a study population of 8.4 million people. PLoS One. 2013;8(11):e79649.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kashipazha D, Mohammadianinejad SE, Majdinasab N, Azizi M, Jafari M. A descriptive study of prevalence, clinical features and other findings of neuromyelitis optica and neuromyelitis optica spectrum disorder in Khuzestan Province, Iran. Iran J Neurol. 2015;14(4):204–10.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Papp V, Illes Z, Magyari M, Koch-Henriksen N, Kant M, Pfleger CC, et al. Nationwide prevalence and incidence study of neuromyelitis optica spectrum disorder in Denmark. Neurology. 2018;91(24):e2265–75.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Wingerchuk DM, Weinshenker BG. Neuromyelitis optica (Devic’s syndrome). Handb Clin Neurol. 2014;122:581–99.CrossRefGoogle Scholar
  16. 16.
    Miller DH, Weinshenker BG, Filippi M, Banwell BL, Cohen JA, Freedman MS, et al. Differential diagnosis of suspected multiple sclerosis: a consensus approach. Mult Scler. 2008;14(9):1157–74.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Fukazawa T, Kikuchi S, Sasaki H, Yabe I, Miyagishi R, Hamada T, et al. Genomic HLA profiles of MS in Hokkaido, Japan: important role of DPB1∗0501 allele. J Neurol. 2000;247(3):175–8.CrossRefGoogle Scholar
  18. 18.
    Nakashima I, Fujihara K, Takase S, Itoyama Y. Decrease in multiple sclerosis with acute transverse myelitis in Japan. Tohoku J Exp Med. 1999;188(1):89–94.CrossRefGoogle Scholar
  19. 19.
    Siritho S, Nakashima I, Takahashi T, Fujihara K, Prayoonwiwat N. AQP4 antibody-positive Thai cases: clinical features and diagnostic problems. Neurology. 2011;77(9):827–34.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Das A, Puvanendran K. A retrospective review of patients with clinically definite multiple sclerosis. Ann Acad Med Singap. 1998;27(2):204–9.PubMedGoogle Scholar
  21. 21.
    Gangopadhyay G, Das SK, Sarda P, Saha SP, Gangopadhyay PK, Roy TN, et al. Clinical profile of multiple sclerosis in Bengal. Neurol India. 1999;47(1):18–21.PubMedGoogle Scholar
  22. 22.
    Kira J-I. Multiple sclerosis in the Japanese population. Lancet Neurol. 2003;2(2):117–27.CrossRefPubMedGoogle Scholar
  23. 23.
    Wingerchuk DM. Neuromyelitis optica: effect of gender. J Neurol Sci. 2009;286(1–2):18–23.CrossRefPubMedGoogle Scholar
  24. 24.
    Kitley J, Leite MI, Kuker W, Quaghebeur G, George J, Waters P, et al. Longitudinally extensive transverse myelitis with and without aquaporin 4 antibodies. JAMA Neurol. 2013;70(11):1375–81.CrossRefPubMedGoogle Scholar
  25. 25.
    Sato DK, Callegaro D, Lana-Peixoto MA, Waters PJ, de Haidar Jorge FM, Takahashi T, et al. Distinction between MOG antibody-positive and AQP4 antibody-positive NMO spectrum disorders. Neurology. 2014;82(6):474–81.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Guimaraaes Brum D, Barreira AA, dos Santos AC, Kaimen-Maciel DR, Matiello M, Costa RM, et al. HLA-DRB association in neuromyelitis optica is different from that observed in multiple sclerosis. Mult Scler J. 2009;16(1):21–9.CrossRefGoogle Scholar
  27. 27.
    Zephir H, Fajardy I, Outteryck O, Blanc F, Roger N, Fleury M, et al. Is neuromyelitis optica associated with human leukocyte antigen? Mult Scler. 2009;15(5):571–9.CrossRefGoogle Scholar
  28. 28.
    Graves J, Grandhe S, Weinfurtner K, Krupp L, Belman A, Chitnis T, et al. Protective environmental factors for neuromyelitis optica. Neurology. 2014;83(21):1923–9.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Simon KC, Schmidt H, Loud S, Ascherio A. Risk factors for multiple sclerosis, neuromyelitis optica and transverse myelitis. Mult Scler. 2015;21(6):703–9.CrossRefGoogle Scholar
  30. 30.
    Estiasari R, Matsushita T, Masaki K, Akiyama T, Yonekawa T, Isobe N, et al. Comparison of clinical, immunological and neuroimaging features between anti-aquaporin-4 antibody-positive and antibody-negative Sjogren’s syndrome patients with central nervous system manifestations. Mult Scler. 2012;18(6):807–16.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Shahmohammadi S, Doosti R, Shahmohammadi A, Mohammadianinejad SE, Sahraian MA, Azimi AR, et al. Autoimmune diseases associated with Neuromyelitis Optica Spectrum disorders: a literature review. Mult Scler Relat Disord. 2019;27:350–63.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Wingerchuk DM, Weinshenker BG. The emerging relationship between neuromyelitis optica and systemic rheumatologic autoimmune disease. Mult Scler. 2012;18(1):5–10.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Wang X, Yi H, Liu J, Li M, Mao ZF, Xu L, et al. Anti-thyroid antibodies and thyroid function in neuromyelitis optica spectrum disorders. J Neurol Sci. 2016;366:3–7.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Niu D, Kondo T, Nakazawa T, Kawasaki T, Yamane T, Mochizuki K, et al. Differential expression of aquaporins and its diagnostic utility in thyroid cancer. PLoS One. 2012;7(7):e40770.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Zoccarato M, Saddi MV, Serra G, Pelizza MF, Rosellini I, Peddone L, et al. Aquaporin-4 antibody neuromyelitis optica following anti-NMDA receptor encephalitis. J Neurol. 2013;260(12):3185–7.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Papadopoulos MC, Manley GT, Krishna S, Verkman AS. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 2004;18(11):1291–3.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Oshio K, Binder DK, Yang B, Schecter S, Verkman AS, Manley GT. Expression of aquaporin water channels in mouse spinal cord. Neuroscience. 2004;127(3):685–93.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Nagelhus EA, Veruki ML, Torp R, Haug FM, Laake JH, Nielsen S, et al. Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Muller cells and fibrous astrocytes. J Neurosci. 1998;18(7):2506–19.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, et al. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet. 2004;364(9451):2106–12.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci. 1997;17(1):171–80.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Bennett JL, Lam C, Kalluri SR, Saikali P, Bautista K, Dupree C, et al. Intrathecal pathogenic anti-aquaporin-4 antibodies in early neuromyelitis optica. Ann Neurol. 2009;66(5):617–29.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Zhang H, Verkman AS. Eosinophil pathogenicity mechanisms and therapeutics in neuromyelitis optica. J Clin Invest. 2013;123(5):2306–16.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Kawachi I, Lassmann H. Neurodegeneration in multiple sclerosis and neuromyelitis optica. J Neurol Neurosurg Psychiatry. 2017;88(2):137–45.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Misu T, Hoftberger R, Fujihara K, Wimmer I, Takai Y, Nishiyama S, et al. Presence of six different lesion types suggests diverse mechanisms of tissue injury in neuromyelitis optica. Acta Neuropathol. 2013;125(6):815–27.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kim HJ, Paul F, Lana-Peixoto MA, Tenembaum S, Asgari N, Palace J, et al. MRI characteristics of neuromyelitis optica spectrum disorder: an international update. Neurology. 2015;84(11):1165–73.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG. The spectrum of neuromyelitis optica. Lancet Neurol. 2007;6(9):805–15.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Rao NA. Chronic experimental allergic optic neuritis. Invest Ophthalmol Vis Sci. 1981;20(2):159–72.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Guy J, Rao NA. Acute and chronic experimental optic neuritis. Alteration in the blood-optic nerve barrier. Arch Ophthalmol. 1984;102(3):450–4.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Butter C, Baker D, O’Neill JK, Turk JL. Mononuclear cell trafficking and plasma protein extravasation into the CNS during chronic relapsing experimental allergic encephalomyelitis in Biozzi AB/H mice. J Neurol Sci. 1991;104(1):9–12.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Popescu BF, Lennon VA, Parisi JE, Howe CL, Weigand SD, Cabrera-Gomez JA, et al. Neuromyelitis optica unique area postrema lesions: nausea, vomiting, and pathogenic implications. Neurology. 2011;76(14):1229–37.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Jiao Y, Fryer JP, Lennon VA, Jenkins SM, Quek AM, Smith CY, et al. Updated estimate of AQP4-IgG serostatus and disability outcome in neuromyelitis optica. Neurology. 2013;81(14):1197–204.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG. Revised diagnostic criteria for neuromyelitis optica. Neurology. 2006;66(10):1485–9.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Wingerchuk DM, Hogancamp WF, O’Brien PC, Weinshenker BG. The clinical course of neuromyelitis optica (Devic’s syndrome). Neurology. 1999;53(5):1107–14.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Flanagan EP, Weinshenker BG, Krecke KN, Pittock SJ. Asymptomatic myelitis in neuromyelitis optica and autoimmune aquaporin-4 channelopathy. Neurol Clin Pract. 2015;5(2):175–7.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kleiter I, Gahlen A, Borisow N, Fischer K, Wernecke KD, Wegner B, et al. Neuromyelitis optica: evaluation of 871 attacks and 1,153 treatment courses. Ann Neurol. 2016;79(2):206–16.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Wingerchuk DM, Pittock SJ, Lucchinetti CF, Lennon VA, Weinshenker BG. A secondary progressive clinical course is uncommon in neuromyelitis optica. Neurology. 2007;68(8):603–5.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Flanagan EP, Weinshenker BG, Krecke KN, Lennon VA, Lucchinetti CF, McKeon A, et al. Short myelitis lesions in aquaporin-4-IgG-positive neuromyelitis optica spectrum disorders. JAMA Neurol. 2015;72(1):81–7.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Weinshenker BG, Wingerchuk DM, Vukusic S, Linbo L, Pittock SJ, Lucchinetti CF, et al. Neuromyelitis optica IgG predicts relapse after longitudinally extensive transverse myelitis. Ann Neurol. 2006;59(3):566–9.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Kanamori Y, Nakashima I, Takai Y, Nishiyama S, Kuroda H, Takahashi T, et al. Pain in neuromyelitis optica and its effect on quality of life: a cross-sectional study. Neurology. 2011;77(7):652–8.CrossRefGoogle Scholar
  61. 61.
    Kim SM, Go MJ, Sung JJ, Park KS, Lee KW. Painful tonic spasm in neuromyelitis optica: incidence, diagnostic utility, and clinical characteristics. Arch Neurol. 2012;69(8):1026–31.CrossRefGoogle Scholar
  62. 62.
    Al-Araji AH, Oger J. Reappraisal of Lhermitte’s sign in multiple sclerosis. Mult Scler. 2005;11(4):398–402.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Hyun JW, Jeong IH, Joung A, Kim SH, Kim HJ. Evaluation of the 2015 diagnostic criteria for neuromyelitis optica spectrum disorder. Neurology. 2016;86(19):1772–9.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Kitley J, Leite MI, Nakashima I, Waters P, McNeillis B, Brown R, et al. Prognostic factors and disease course in aquaporin-4 antibody-positive patients with neuromyelitis optica spectrum disorder from the United Kingdom and Japan. Brain. 2012;135(6):1834–49.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Storoni M, Davagnanam I, Radon M, Siddiqui A, Plant GT. Distinguishing optic neuritis in neuromyelitis optica spectrum disease from multiple sclerosis: a novel magnetic resonance imaging scoring system. J Neuroophthalmol. 2013;33(2):123–7.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Khanna S, Sharma A, Huecker J, Gordon M, Naismith RT, Van Stavern GP. Magnetic resonance imaging of optic neuritis in patients with neuromyelitis optica versus multiple sclerosis. J Neuroophthalmol. 2012;32(3):216–20.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Costa RM, Santos AC, Costa LS. An unusual chiasmal visual defect in a patient with neuromyelitis optica: case report. Arq Bras Oftalmol. 2007;70(1):153–5.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Raz N, Vaknin A, Chokron S, Ben-Hur T, Levin N. Functional MRI as a tool for assessing chiasmal visual defect in a patient with neuromyelitis optica. J Neurol Neurosurg Psychiatry. 2010;81(10):1174–5.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Papais-Alvarenga RM, Carellos SC, Alvarenga MP, Holander C, Bichara RP, Thuler LC. Clinical course of optic neuritis in patients with relapsing neuromyelitis optica. Arch Ophthalmol. 2008;126(1):12–6.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Matiello M, Lennon VA, Jacob A, Pittock SJ, Lucchinetti CF, Wingerchuk DM, et al. NMO-IgG predicts the outcome of recurrent optic neuritis. Neurology. 2008;70(23):2197–200.CrossRefGoogle Scholar
  71. 71.
    Misu T, Fujihara K, Nakashima I, Sato S, Itoyama Y. Intractable hiccup and nausea with periaqueductal lesions in neuromyelitis optica. Neurology. 2005;65(9):1479–82.CrossRefGoogle Scholar
  72. 72.
    Kremer L, Mealy M, Jacob A, Nakashima I, Cabre P, Bigi S, et al. Brainstem manifestations in neuromyelitis optica: a multicenter study of 258 patients. Mult Scler. 2014;20(7):843–7.CrossRefGoogle Scholar
  73. 73.
    Kallollimath P, Gujjar A, Patil M. Symptomatic narcolepsy as a presenting feature of neuromyelitis optica. Ann Indian Acad Neurol. 2018;21(2):156–8.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Carlander B, Vincent T, Le Floch A, Pageot N, Camu W, Dauvilliers Y. Hypocretinergic dysfunction in neuromyelitis optica with coma-like episodes. BMJ Case Rep. 2009;2009.Google Scholar
  75. 75.
    Suzuki K, Nakamura T, Hashimoto K, Miyamoto M, Komagamine T, Nagashima T, et al. Hypothermia, hypotension, hypersomnia, and obesity associated with hypothalamic lesions in a patient positive for the anti-aquaporin 4 antibody: a case report and literature review. Arch Neurol. 2012;69(10):1355–9.CrossRefGoogle Scholar
  76. 76.
    Iorio R, Plantone D, Damato V, Paola Batocchi A. Anorexia heralding the onset of neuromyelitis optica. Intern Med. 2013;52(4):489–91.CrossRefGoogle Scholar
  77. 77.
    Pu S, Long Y, Yang N, He Y, Shan F, Fan Y, et al. Syndrome of inappropriate antidiuretic hormone secretion in patients with aquaporin-4 antibody. J Neurol. 2015;262(1):101–7.CrossRefGoogle Scholar
  78. 78.
    Kim W, Kim SH, Lee SH, Li XF, Kim HJ. Brain abnormalities as an initial manifestation of neuromyelitis optica spectrum disorder. Mult Scler. 2011;17(9):1107–12.CrossRefGoogle Scholar
  79. 79.
    Magana SM, Matiello M, Pittock SJ, McKeon A, Lennon VA, Rabinstein AA, et al. Posterior reversible encephalopathy syndrome in neuromyelitis optica spectrum disorders. Neurology. 2009;72(8):712–7.CrossRefGoogle Scholar
  80. 80.
    Newey CR, Bermel RA. Fulminant cerebral demyelination in neuromyelitis optica. Neurology. 2011;77(2):193.CrossRefGoogle Scholar
  81. 81.
    Jia K, Zhang X, Zhang LJ, Li LM, Qi Y, Yi M, et al. Anti-neurofascin-155 antibody-positive neuromyelitis optica spectrum disorders. J Neurol Sci. 2019;398:16–8.CrossRefGoogle Scholar
  82. 82.
    Abboud H, Fernandez HH, Mealy MA, Levy M. Spinal movement disorders in neuromyelitis optica: an under-recognized phenomenon. Mov Disord Clin Pract. 2016;3(6):596–602.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Usmani N, Bedi G, Lam BL, Sheremata WA. Association between paroxysmal tonic spasms and neuromyelitis optica. Arch Neurol. 2012;69(1):121–4.CrossRefGoogle Scholar
  84. 84.
    Bradl M, Kanamori Y, Nakashima I, Misu T, Fujihara K, Lassmann H, et al. Pain in neuromyelitis optica—prevalence, pathogenesis and therapy. Nat Rev Neurol. 2014;10(9):529–36.CrossRefGoogle Scholar
  85. 85.
    Xiao L, Qiu W, Lu Z, Li R, Hu X. Intractable pruritus in neuromyelitis optica. Neurol Sci. 2016 Jun;37(6):949–54.CrossRefGoogle Scholar
  86. 86.
    Netravathi M, Saini J, Mahadevan A, Hari-Krishna B, Yadav R, Pal PK, et al. Is pruritus an indicator of aquaporin-positive neuromyelitis optica? Mult Scler. 2017;23(6):810–7.CrossRefGoogle Scholar
  87. 87.
    Wingerchuk DM, Weinshenker BG. Neuromyelitis optica: clinical predictors of a relapsing course and survival. Neurology. 2003;60(5):848–53.CrossRefGoogle Scholar
  88. 88.
    Bulut E, Karakaya J, Salama S, Levy M, Huisman T, Izbudak I. Brain MRI findings in pediatric-onset neuromyelitis optica spectrum disorder: challenges in differentiation from acute disseminated encephalomyelitis. AJNR Am J Neuroradiol. 2019;40(4):726–31.PubMedGoogle Scholar
  89. 89.
    McKeon A, Lennon VA, Lotze T, Tenenbaum S, Ness JM, Rensel M, et al. CNS aquaporin-4 autoimmunity in children. Neurology. 2008;71(2):93–100.CrossRefGoogle Scholar
  90. 90.
    Annus A, Bencsik K, Obal I, Kincses ZT, Tiszlavicz L, Hoftberger R, et al. Paraneoplastic neuromyelitis optica spectrum disorder: a case report and review of the literature. J Clin Neurosci. 2018;48:7–10.CrossRefGoogle Scholar
  91. 91.
    Chan KH, Kwan JS, Ho PW, Ho SL, Chui WH, Chu AC, et al. Aquaporin-4 water channel expression by thymoma of patients with and without myasthenia gravis. J Neuroimmunol. 2010;227(1–2):178–84.CrossRefGoogle Scholar
  92. 92.
    Warth A, Simon P, Capper D, Goeppert B, Tabatabai G, Herzog H, et al. Expression pattern of the water channel aquaporin-4 in human gliomas is associated with blood-brain barrier disturbance but not with patient survival. J Neurosci Res. 2007;85(6):1336–46.CrossRefGoogle Scholar
  93. 93.
    Armagan H, Tuzun E, Icoz S, Birisik O, Ulusoy C, Demir G, et al. Long extensive transverse myelitis associated with aquaporin-4 antibody and breast cancer: favorable response to cancer treatment. J Spinal Cord Med. 2012;35(4):267–9.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Warth A, Muley T, Meister M, Herpel E, Pathil A, Hoffmann H, et al. Loss of aquaporin-4 expression and putative function in non-small cell lung cancer. BMC Cancer. 2011;11:161.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Cai G, He D, Chu L, Dai Q, Xu Z, Zhang Y. Paraneoplastic neuromyelitis optica spectrum disorders: three new cases and a review of the literature. Int J Neurosci. 2016;126(7):660–8.PubMedGoogle Scholar
  96. 96.
    Lycklama G, Thompson A, Filippi M, Miller D, Polman C, Fazekas F, et al. Spinal-cord MRI in multiple sclerosis. Lancet Neurol. 2003;2(9):555–62.CrossRefGoogle Scholar
  97. 97.
    Tartaglino LM, Friedman DP, Flanders AE, Lublin FD, Knobler RL, Liem M. Multiple sclerosis in the spinal cord: MR appearance and correlation with clinical parameters. Radiology. 1995;195(3):725–32.CrossRefGoogle Scholar
  98. 98.
    Cacciaguerra L, Meani A, Mesaros S, Radaelli M, Palace J, Dujmovic-Basuroski I, et al. Brain and cord imaging features in neuromyelitis optica spectrum disorders. Ann Neurol. 2019;85(3):371–84.CrossRefGoogle Scholar
  99. 99.
    Sand IK. Neuromyelitis optica spectrum disorders. Continuum (Minneap Minn). 2016;22(3):864–96.Google Scholar
  100. 100.
    Petzold A, Wattjes MP, Costello F, Flores-Rivera J, Fraser CL, Fujihara K, et al. The investigation of acute optic neuritis: a review and proposed protocol. Nat Rev Neurol. 2014;10(8):447–58.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Jarius S, Aboul-Enein F, Waters P, Kuenz B, Hauser A, Berger T, et al. Antibody to aquaporin-4 in the long-term course of neuromyelitis optica. Brain. 2008;131(Pt 11):3072–80.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Jarius S, Wildemann B. The history of neuromyelitis optica. J Neuroinflammation. 2013;10:8.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Kitley J, Woodhall M, Waters P, Leite MI, Devenney E, Craig J, et al. Myelin-oligodendrocyte glycoprotein antibodies in adults with a neuromyelitis optica phenotype. Neurology. 2012;79(12):1273–7.CrossRefGoogle Scholar
  104. 104.
    Sechi E, Flanagan EP. Area postrema syndrome in autoimmune GFAP astrocytopathy. Mult Scler. 2019:1352458519826489.Google Scholar
  105. 105.
    Sechi E, Morris PP, McKeon A, Pittock SJ, Hinson SR, Weinshenker BG, et al. Glial fibrillary acidic protein IgG related myelitis: characterisation and comparison with aquaporin-4-IgG myelitis. J Neurol Neurosurg Psychiatry. 2019;90(4):488–90.CrossRefPubMedGoogle Scholar
  106. 106.
    Jarius S, Paul F, Franciotta D, Ruprecht K, Ringelstein M, Bergamaschi R, et al. Cerebrospinal fluid findings in aquaporin-4 antibody positive neuromyelitis optica: results from 211 lumbar punctures. J Neurol Sci. 2011;306(1–2):82–90.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Uzawa A, Mori M, Sawai S, Masuda S, Muto M, Uchida T, et al. Cerebrospinal fluid interleukin-6 and glial fibrillary acidic protein levels are increased during initial neuromyelitis optica attacks. Clin Chim Acta. 2013;421:181–3.CrossRefPubMedGoogle Scholar
  108. 108.
    Nakamura M, Miyazawa I, Fujihara K, Nakashima I, Misu T, Watanabe S, et al. Preferential spinal central gray matter involvement in neuromyelitis optica. J Neurol. 2008;255(2):163–70.CrossRefPubMedGoogle Scholar
  109. 109.
    Murchison A, Kitley J, Leite MI, Kuker W, Palace J. Predictive value of MRI parameters in severity and recovery of first-episode myelitis in aquaporin-4 antibody disease. J Neurol Sci. 2015;355(1–2):49–53.CrossRefPubMedGoogle Scholar
  110. 110.
    Yonezu T, Ito S, Mori M, Ogawa Y, Makino T, Uzawa A, et al. “Bright spotty lesions” on spinal magnetic resonance imaging differentiate neuromyelitis optica from multiple sclerosis. Mult Scler. 2014;20(3):331–7.CrossRefGoogle Scholar
  111. 111.
    Asgari N, Skejoe HP, Lillevang ST, Steenstrup T, Stenager E, Kyvik KO. Modifications of longitudinally extensive transverse myelitis and brainstem lesions in the course of neuromyelitis optica (NMO): a population-based, descriptive study. BMC Neurol. 2013;13:33.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Kim W, Min Su P, Sang Hyun L, Kim SH, Jung IJ, Takahashi T, et al. Characteristic brain magnetic resonance imaging abnormalities in central nervous system aquaporin-4 autoimmunity. Mult Scler. 2010;16(10):1229–36.CrossRefGoogle Scholar
  113. 113.
    Nakamura M, Misu T, Fujihara K, Miyazawa I, Nakashima I, Takahashi T, et al. Occurrence of acute large and edematous callosal lesions in neuromyelitis optica. Mult Scler. 2009;15(6):695–700.CrossRefGoogle Scholar
  114. 114.
    Makino T, Ito S, Mori M, Yonezu T, Ogawa Y, Kuwabara S. Diffuse and heterogeneous T2-hyperintense lesions in the splenium are characteristic of neuromyelitis optica. Mult Scler. 2013;19(3):308–15.CrossRefGoogle Scholar
  115. 115.
    Pittock SJ, Weinshenker BG, Lucchinetti CF, Wingerchuk DM, Corboy JR, Lennon VA. Neuromyelitis optica brain lesions localized at sites of high aquaporin 4 expression. Arch Neurol. 2006;63(7):964–8.CrossRefGoogle Scholar
  116. 116.
    Matsushita T, Isobe N, Matsuoka T, Ishizu T, Kawano Y, Yoshiura T, et al. Extensive vasogenic edema of anti-aquaporin-4 antibody-related brain lesions. Mult Scler. 2009;15(9):1113–7.CrossRefGoogle Scholar
  117. 117.
    Ito S, Mori M, Makino T, Hayakawa S, Kuwabara S. “Cloud-like enhancement” is a magnetic resonance imaging abnormality specific to neuromyelitis optica. Ann Neurol. 2009;66(3):425–8.CrossRefGoogle Scholar
  118. 118.
    Banker P, Sonni S, Kister I, Loh JP, Lui YW. Pencil-thin ependymal enhancement in neuromyelitis optica spectrum disorders. Mult Scler. 2012;18(7):1050–3.CrossRefGoogle Scholar
  119. 119.
    Kim W, Kim SH, Huh SY, Kim HJ. Brain abnormalities in neuromyelitis optica spectrum disorder. Mult Scler Int. 2012;2012:735486.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Calabrese M, Oh MS, Favaretto A, Rinaldi F, Poretto V, Alessio S, et al. No MRI evidence of cortical lesions in neuromyelitis optica. Neurology. 2012;79(16):1671–6.CrossRefGoogle Scholar
  121. 121.
    Biswas A, Mukherjee A. Therapy of NMO spectrum disorders. Ann Indian Acad Neurol. 2015;18(Suppl 1):S16–23.PubMedPubMedCentralGoogle Scholar
  122. 122.
    Elsone L, Panicker J, Mutch K, Boggild M, Appleton R, Jacob A. Role of intravenous immunoglobulin in the treatment of acute relapses of neuromyelitis optica: experience in 10 patients. Mult Scler. 2014;20(4):501–4.CrossRefGoogle Scholar
  123. 123.
    Abboud H, Petrak A, Mealy M, Sasidharan S, Siddique L, Levy M. Treatment of acute relapses in neuromyelitis optica: steroids alone versus steroids plus plasma exchange. Mult Scler. 2016;22(2):185–92.CrossRefGoogle Scholar
  124. 124.
    Kleiter I, Gahlen A, Borisow N, Fischer K, Wernecke KD, Hellwig K, et al. Apheresis therapies for NMOSD attacks: a retrospective study of 207 therapeutic interventions. Neurol Neuroimmunol Neuroinflamm. 2018;5(6):e504.CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Bonnan M, Valentino R, Debeugny S, Merle H, Ferge JL, Mehdaoui H, et al. Short delay to initiate plasma exchange is the strongest predictor of outcome in severe attacks of NMO spectrum disorders. J Neurol Neurosurg Psychiatry. 2018;89(4):346–51.CrossRefGoogle Scholar
  126. 126.
    Kim SH, Kim W, Li XF, Jung IJ, Kim HJ. Does interferon beta treatment exacerbate neuromyelitis optica spectrum disorder? Mult Scler. 2012;18(10):1480–3.CrossRefGoogle Scholar
  127. 127.
    Gahlen A, Trampe AK, Haupeltshofer S, Ringelstein M, Aktas O, Berthele A, et al. Aquaporin-4 antibodies in patients treated with natalizumab for suspected MS. Neurol Neuroimmunol Neuroinflamm. 2017;4(4):e363.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Chen H, Qiu W, Zhang Q, Wang J, Shi Z, Liu J, et al. Comparisons of the efficacy and tolerability of mycophenolate mofetil and azathioprine as treatments for neuromyelitis optica and neuromyelitis optica spectrum disorder. Eur J Neurol. 2017;24(1):219–26.CrossRefGoogle Scholar
  129. 129.
    Nikoo Z, Badihian S, Shaygannejad V, Asgari N, Ashtari F. Comparison of the efficacy of azathioprine and rituximab in neuromyelitis optica spectrum disorder: a randomized clinical trial. J Neurol. 2017;264(9):2003–9.CrossRefGoogle Scholar
  130. 130.
    Jeong IH, Park B, Kim SH, Hyun JW, Joo J, Kim HJ. Comparative analysis of treatment outcomes in patients with neuromyelitis optica spectrum disorder using multifaceted endpoints. Mult Scler. 2016;22(3):329–39.CrossRefGoogle Scholar
  131. 131.
    Mandler RN, Ahmed W, Dencoff JE. Devic’s neuromyelitis optica: a prospective study of seven patients treated with prednisone and azathioprine. Neurology. 1998;51(4):1219–20.CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Kimbrough DJ, Fujihara K, Jacob A, Lana-Peixoto MA, Isabel Leite M, Levy M, et al. Treatment of neuromyelitis optica: review and recommendations. Mult Scler Relat Disord. 2012;1(4):180–7.CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Mealy MA, Wingerchuk DM, Palace J, Greenberg BM, Levy M. Comparison of relapse and treatment failure rates among patients with neuromyelitis optica: multicenter study of treatment efficacy. JAMA Neurol. 2014;71(3):324–30.CrossRefPubMedPubMedCentralGoogle Scholar
  134. 134.
    Cree BAC, Lamb S, Morgan K, Chen A, Waubant E, Genain C. An open label study of the effects of rituximab in neuromyelitis optica. Neurology. 2005;64(7):1270–2.CrossRefPubMedPubMedCentralGoogle Scholar
  135. 135.
    Kim SH, Huh SY, Lee SJ, Joung A, Kim HJ. A 5-year follow-up of rituximab treatment in patients with neuromyelitis optica spectrum disorder. JAMA Neurol. 2013;70(9):1110–7.CrossRefPubMedPubMedCentralGoogle Scholar
  136. 136.
    Kim SH, Kim W, Li XF, Jung IJ, Kim HJ. Repeated treatment with rituximab based on the assessment of peripheral circulating memory B cells in patients with relapsing neuromyelitis optica over 2 years. Arch Neurol. 2011;68(11):1412–20.CrossRefPubMedPubMedCentralGoogle Scholar
  137. 137.
    Jacob A, Weinshenker BG, Violich I, McLinskey N, Krupp L, Fox RJ, et al. Treatment of neuromyelitis optica with rituximab: retrospective analysis of 25 patients. Arch Neurol. 2008;65(11):1443–8.CrossRefPubMedPubMedCentralGoogle Scholar
  138. 138.
    Bedi GS, Brown AD, Delgado SR, Usmani N, Lam BL, Sheremata WA. Impact of rituximab on relapse rate and disability in neuromyelitis optica. Mult Scler. 2011;17(10):1225–30.CrossRefPubMedPubMedCentralGoogle Scholar
  139. 139.
    Zephir H, Bernard-Valnet R, Lebrun C, Outteryck O, Audoin B, Bourre B, et al. Rituximab as first-line therapy in neuromyelitis optica: efficiency and tolerability. J Neurol. 2015;262(10):2329–35.CrossRefPubMedPubMedCentralGoogle Scholar
  140. 140.
    Nakashima I, Takahashi T, Cree BA, Kim HJ, Suzuki C, Genain CP, et al. Transient increases in anti-aquaporin-4 antibody titers following rituximab treatment in neuromyelitis optica, in association with elevated serum BAFF levels. J Clin Neurosci. 2011;18(7):997–8.CrossRefPubMedPubMedCentralGoogle Scholar
  141. 141.
    Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med. 2004;350(25):2572–81.CrossRefPubMedPubMedCentralGoogle Scholar
  142. 142.
    Annovazzi P, Capobianco M, Moiola L, Patti F, Frau J, Uccelli A, et al. Rituximab in the treatment of neuromyelitis optica: a multicentre Italian observational study. J Neurol. 2016;263(9):1727–35.CrossRefGoogle Scholar
  143. 143.
    Yang CS, Yang L, Li T, Zhang DQ, Jin WN, Li MS, et al. Responsiveness to reduced dosage of rituximab in Chinese patients with neuromyelitis optica. Neurology. 2013;81(8):710–3.CrossRefPubMedPubMedCentralGoogle Scholar
  144. 144.
    Pittock SJ, Berthele A, Fujihara K, Kim HJ, Levy M, Palace J, et al. Eculizumab in aquaporin-4-positive neuromyelitis optica spectrum disorder. N Engl J Med. 2019;381(7):614–25.CrossRefGoogle Scholar
  145. 145.
    Ringelstein M, Ayzenberg I, Harmel J, Lauenstein AS, Lensch E, Stogbauer F, et al. Long-term therapy with interleukin 6 receptor blockade in highly active neuromyelitis optica spectrum disorder. JAMA Neurol. 2015;72(7):756–63.CrossRefGoogle Scholar
  146. 146.
    Zhang C, Tian DC, Yang CS, Han B, Wang J, Yang L, et al. Safety and efficacy of bortezomib in patients with highly relapsing neuromyelitis optica spectrum disorder. JAMA Neurol. 2017;74(8):1010–2.CrossRefPubMedPubMedCentralGoogle Scholar
  147. 147.
    Burman J, Tolf A, Hagglund H, Askmark H. Autologous haematopoietic stem cell transplantation for neurological diseases. J Neurol Neurosurg Psychiatry. 2018;89(2):147–55.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Massimo Filippi
    • 1
    • 2
    • 3
    • 4
  • Maria A. Rocca
    • 2
  1. 1.Neurology UnitIRCCS San Raffaele Scientific InstituteMilanoItaly
  2. 2.Neuroimaging Research UnitIRCCS San Raffaele Scientific InstituteMilanoItaly
  3. 3.Neurophysiology UnitIRCCS San Raffaele Scientific InstituteMilanoItaly
  4. 4.Vita-Salute San Raffaele UniversityMilanoItaly

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