Top

Published in:

01-10-2015 | Original Communication

Features of anti-aquaporin 4 antibody-seropositive Chinese patients with neuromyelitis optica spectrum optic neuritis

Authors: Hongyang Li, Yanling Wang, Quangang Xu, Aidi Zhang, Huanfen Zhou, Shuo Zhao, Hao Kang, Chunxia Peng, Shanshan Cao, Shihui Wei

Published in: Journal of Neurology | Issue 10/2015

Abstract

The detection of anti-aquaporin-4 autoantibody (AQP-4 Ab) is crucial to detect patients who will develop neuromyelitis optica (NMO); however, there are few studies on the AQP-4 Ab serostatus of patients with neuromyelitis optica spectrum ON. We analyzed the clinical and paraclinical features of neuromyelitis optica spectrum ON patients in China according to the patients’ AQP4-Ab serostatus. 125 patients with recurrent and bilateral ON with simultaneous attacks were divided into AQP-4 Ab-seropositive and -seronegative groups. Demographic, clinical, serum autoantibody data, connective tissue disorders (CTDs), visual performance were compared. A Visual Acuity (VA) of less than 0.1 during acute ON attacks occurred more frequently in the seropositive group (p = 0.023); however, there was not a significant difference between groups on VA recovery after the first attack. The seropositive group experienced the worst outcome during the last attack (p = 0.017). Other co-existing autoimmunity antibodies (p < 0.001) and CTDs (p < 0.001) were more prevalent in seropositive patients. There were no significant differences on VA recovery and RNFLT combined with other autoantibodies or CTDs. The two groups did not differ significantly with regard to time to relapse, annualized relapse rates, time of diagnosis NMO, or RNFL. There were no significant differences on VA recovery and RNFLT combined with other autoantibodies or CTDs. RNFLT was thinner in NMO seropositive patients. Although AQP-4 Ab expression predicted poor visual outcome, positive patients were usually associated with mild symptoms at first onset. Anti-SSA/SSB antibody or Sjögren syndrome may be associated with AQP-4 Ab in neuromyelitis optica spectrum ON.

Beck RW, Cleary PA, Anderson MM Jr, Keltner JL, Shults WT, Kaufman DI, Buckley EG, Corbett JJ, Kupersmith MJ, Miller NR et al (1992) A randomized, controlled trial of corticosteroids in the treatment of acute optic neuritis. The Optic Neuritis Study Group. N Eng J Med 326(9):581–588CrossRef

Hickman SJ, Dalton CM, Miller DH, Plant GT (2002) Management of acute optic neuritis. Lancet 360(9349):1953–1962CrossRefPubMed

Shimizu J, Hatanaka Y, Hasegawa M, Iwata A, Sugimoto I, Date H, Goto J, Shimizu T, Takatsu M, Sakurai Y et al (2010) IFNbeta-1b may severely exacerbate Japanese optic-spinal MS in neuromyelitis optica spectrum. Neurology 75(16):1423–1427CrossRefPubMed

McKeon A, Fryer JP, Apiwattanakul M, Lennon VA, Hinson SR, Kryzer TJ, Lucchinetti CF, Weinshenker BG, Wingerchuk DM, Shuster EA et al (2009) Diagnosis of neuromyelitis spectrum disorders: comparative sensitivities and specificities of immunohistochemical and immunoprecipitation assays. Arch Neurol 66(9):1134–1138CrossRefPubMed

Takahashi T, Fujihara K, Nakashima I, Misu T, Miyazawa I, Nakamura M, Watanabe S, Shiga Y, Kanaoka C, Fujimori J et al (2007) Anti-aquaporin-4 antibody is involved in the pathogenesis of NMO: a study on antibody titre. Brain J Neurol 130(Pt 5):1235–1243CrossRef

Costa C, Arrambide G, Tintore M, Castillo J, Sastre-Garriga J, Tur C, Rio J, Saiz A, Vidal-Jordana A, Auger C et al (2012) Value of NMO-IgG determination at the time of presentation as CIS. Neurology 78(20):1608–1611CrossRefPubMed

Akman-Demir G, Tuzun E, Waters P, Icoz S, Kurtuncu M, Jarius S, Yapici Z, Mutlu M, Yesilot N, Vincent A et al (2011) Prognostic implications of aquaporin-4 antibody status in neuromyelitis optica patients. J Neurol 258(3):464–470CrossRefPubMed

Yang Y, Huang DH, Wu WP, Wu L, Chen LF, Wu Q (2013) The role of aquaporin-4 antibodies in Chinese patients with neuromyelitis optica. J Clin Neurosci 20(1):94–98CrossRefPubMed

Lai C, Tian G, Takahashi T, Liu W, Yang L, Zhang X (2011) Neuromyelitis optica antibodies in patients with severe optic neuritis in China. J Neuro Ophthalmol 31(1):16–19CrossRef

10.

Nakashima I, Fujihara K, Miyazawa I, Misu T, Narikawa K, Nakamura M, Watanabe S, Takahashi T, Nishiyama S, Shiga Y et al (2006) Clinical and MRI features of Japanese patients with multiple sclerosis positive for NMO-IgG. J Neurol Neurosurg Psychiatry 77(9):1073–1075PubMedCentralCrossRefPubMed

11.

Asgari N, Lillevang ST, Skejoe HP, Falah M, Stenager E, Kyvik KO (2011) A population-based study of neuromyelitis optica in Caucasians. Neurology 76(18):1589–1595PubMedCentralCrossRefPubMed

12.

Ghezzi A, Bergamaschi R, Martinelli V, Trojano M, Tola MR, Merelli E, Mancardi L, Gallo P, Filippi M, Zaffaroni M et al (2004) Clinical characteristics, course and prognosis of relapsing Devic’s Neuromyelitis Optica. J Neurol 251(1):47–52CrossRefPubMed

13.

Bichuetti DB, Oliveira EM, Souza NA, Rivero RL, Gabbai AA (2009) Neuromyelitis optica in Brazil: a study on clinical and prognostic factors. Mult Scler 15(5):613–619CrossRefPubMed

14.

Jarius S, Frederikson J, Waters P, Paul F, Akman-Demir G, Marignier R, Franciotta D, Ruprecht K, Kuenz B, Rommer P et al (2010) Frequency and prognostic impact of antibodies to aquaporin-4 in patients with optic neuritis. J Neurol Sci 298(1–2):158–162CrossRefPubMed

15.

Petzold A, Pittock S, Lennon V, Maggiore C, Weinshenker BG, Plant GT (2010) Neuromyelitis optica-IgG (aquaporin-4) autoantibodies in immune mediated optic neuritis. J Neurol Neurosurg Psychiatry 81(1):109–111CrossRefPubMed

16.

Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG (2007) The spectrum of neuromyelitis optica. Lancet Neurol 6(9):805–815CrossRefPubMed

17.

Li H, Zhang Y, Yi Z, Huang D, Wei S (2014) Frequency of autoantibodies and connective tissue diseases in Chinese patients with optic neuritis. PLoS One 9(6):e99323PubMedCentralCrossRefPubMed

18.

Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L et al (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69(2):292–302PubMedCentralCrossRefPubMed

19.

Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66(10):1485–1489CrossRefPubMed

20.

Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO 3rd, Birnbaum NS, Burmester GR, Bykerk VP, Cohen MD et al (2010) 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 62(9):2569–2581CrossRefPubMed

21.

Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, Daniels TE, Fox PC, Fox RI, Kassan SS et al (2002) Classification criteria for Sjogren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 61(6):554–558PubMedCentralCrossRefPubMed

22.

Gan FY, Fei YY, Li MT, Wang Q, Xu D, Hou Y, Zeng XF, Zhang FC (2014) The characteristics of patients having ankylosing spondylitis associated with Takayasu’s arteritis. Clin Rheumatol 33(3):355–358CrossRefPubMed

23.

Castro J, Balada E, Ordi-Ros J, Vilardell-Tarres M (2008) The complex immunogenetic basis of systemic lupus erythematosus. Autoimmun Rev 7(5):345–351CrossRefPubMed

24.

Hoffman GS, Kerr GS, Leavitt RY, Hallahan CW, Lebovics RS, Travis WD, Rottem M, Fauci AS (1992) Wegener granulomatosis: an analysis of 158 patients. Ann Intern Med 116(6):488–498CrossRefPubMed

25.

International Study Group for Behcet’s Disease (1990) Criteria for diagnosis of Behcet’s disease. Lancet 335(8697):1078–1080

26.

Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, Derksen RH, DE Groot PG, Koike T, Meroni PL et al (2006) International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 4(2):295–306CrossRefPubMed

27.

Mader S, Lutterotti A, Di Pauli F, Kuenz B, Schanda K, Aboul-Enein F, Khalil M, Storch MK, Jarius S, Kristoferitsch W et al (2010) Patterns of antibody binding to aquaporin-4 isoforms in neuromyelitis optica. PLoS One 5(5):e10455PubMedCentralCrossRefPubMed

28.

Weinshenker BG, Rice GP, Noseworthy JH, Carriere W, Baskerville J, Ebers GC (1991) The natural history of multiple sclerosis: a geographically based study. 4. Applications to planning and interpretation of clinical therapeutic trials. Brain J Neurol 114(Pt 2):1057–1067CrossRef

29.

Etemadifar M, Abtahi MA, Razmjoo H, Abtahi SH, Dehghani AR, Abtahi ZA, Akbari M, Mazaheri S, Maghzi AH (2012) Anti-aquaporin-4 IgG in patients presenting with unilateral optic neuritis: a cohort study. Int J Prevent Med 3(9):612–615

30.

Hinson SR, McKeon A, Lennon VA (2010) Neurological autoimmunity targeting aquaporin-4. Neuroscience 168(4):1009–1018CrossRefPubMed

31.

Matiello M, Lennon VA, Jacob A, Pittock SJ, Lucchinetti CF, Wingerchuk DM, Weinshenker BG (2008) NMO-IgG predicts the outcome of recurrent optic neuritis. Neurology 70(23):2197–2200CrossRefPubMed

32.

Jarius S, Ruprecht K, Wildemann B, Kuempfel T, Ringelstein M, Geis C, Kleiter I, Kleinschnitz C, Berthele A, Brettschneider J et al (2012) Contrasting disease patterns in seropositive and seronegative neuromyelitis optica: a multicentre study of 175 patients. J Neuroinflammation 9:14PubMedCentralCrossRefPubMed

33.

Koller H, Neuen-Jacob E, Saleh A, Kieseier BC, Jander S, Hartung HP (2006) A patient with a benign course of neuromyelitis optica (Devic’s syndrome) over 12 years: mRI follow up and histological findings. J Neurol 253(6):819–820CrossRefPubMed

34.

Collongues N, Cabre P, Marignier R, Zephir H, Papeix C, Audoin B, Lebrun-Frenay C, Pelletier J, Fontaine B, Vermersch P et al (2011) A benign form of neuromyelitis optica: does it exist? Arch Neurol 68(7):918–924CrossRefPubMed

35.

Burman J, Raininko R, Fagius J (2011) Bilateral and recurrent optic neuritis in multiple sclerosis. Acta Neurol Scand 123(3):207–210CrossRefPubMed

36.

Pirko I, Blauwet LA, Lesnick TG, Weinshenker BG (2004) The natural history of recurrent optic neuritis. Arch Neurol 61(9):1401–1405CrossRefPubMed

37.

Polman CH, Reingold SC, Edan G, Filippi M, Hartung HP, Kappos L, Lublin FD, Metz LM, McFarland HF, O’Connor PW et al (2005) Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Ann Neurol 58(6):840–846CrossRefPubMed

38.

Silva FR, Vidotti VG, Cremasco F, Dias M, Gomi ES, Costa VP (2013) Sensitivity and specificity of machine learning classifiers for glaucoma diagnosis using spectral domain OCT and standard automated perimetry. Arq Bras Oftalmol 76(3):170–174CrossRefPubMed

39.

Garcia-Martin E, Polo V, Larrosa JM, Marques ML, Herrero R, Martin J, Ara JR, Fernandez J, Pablo LE (2014) Retinal layer segmentation in patients with multiple sclerosis using spectral domain optical coherence tomography. Ophthalmology 121(2):573–579CrossRefPubMed

40.

Ratchford JN, Quigg ME, Conger A, Frohman T, Frohman E, Balcer LJ, Calabresi PA, Kerr DA (2009) Optical coherence tomography helps differentiate neuromyelitis optica and MS optic neuropathies. Neurology 73(4):302–308PubMedCentralCrossRefPubMed

41.

Naismith RT, Tutlam NT, Xu J, Klawiter EC, Shepherd J, Trinkaus K, Song SK, Cross AH (2009) Optical coherence tomography differs in neuromyelitis optica compared with multiple sclerosis. Neurology 72(12):1077–1082PubMedCentralCrossRefPubMed

42.

Kardon RH (2011) Role of the macular optical coherence tomography scan in neuro-ophthalmology. J Neuroophthalmol 31(4):353–361PubMedCentralCrossRefPubMed

43.

Adawi M, Bisharat B, Bowirrat A (2014) Systemic Lupus Erythematosus (SLE) complicated by Neuromyelitis Optica (NMO—Devic’s Disease): clinic-pathological report and review of the literature. Clin Me Insights Case Rep 7:41–47

44.

Jayarangaiah A, Sehgal R, Epperla N (2014) Sjogren inverted question marks syndrome and Neuromyelitis Optica spectrum disorders (NMOSD) inverted question mark a case report and review of literature. BMC Neurol 14(1):200PubMedCentralCrossRefPubMed

45.

Javed A, Balabanov R, Arnason BG, Kelly TJ, Sweiss NJ, Pytel P, Walsh R, Blair EA, Stemer A, Lazzaro M et al (2008) Minor salivary gland inflammation in Devic’s disease and longitudinally extensive myelitis. Mult Scler 14(6):809–814CrossRefPubMed

46.

Solomon AJ, Hills W, Chen Z, Rosenbaum J, Bourdette D, Whitham R (2013) Autoantibodies and Sjogren’s Syndrome in multiple sclerosis, a reappraisal. PLoS One 8(6):e65385PubMedCentralCrossRefPubMed

47.

Sandberg-Wollheim M, Axell T, Hansen BU, Henricsson V, Ingesson E, Jacobsson L, Larsson A, Lieberkind K, Manthorpe R (1992) Primary Sjogren’s syndrome in patients with multiple sclerosis. Neurology 42(4):845–847CrossRefPubMed

48.

Jarius S, Franciotta D, Paul F, Ruprecht K, Bergamaschi R, Rommer PS, Reuss R, Probst C, Kristoferitsch W, Wandinger KP et al (2010) Cerebrospinal fluid antibodies to aquaporin-4 in neuromyelitis optica and related disorders: frequency, origin, and diagnostic relevance. J Neuroinflammation 7:52PubMedCentralCrossRefPubMed

49.

Jarius S, Paul F, Franciotta D, Ruprecht K, Ringelstein M, Bergamaschi R, Rommer P, Kleiter I, Stich O, Reuss R et al (2011) Cerebrospinal fluid findings in aquaporin-4 antibody positive neuromyelitis optica: results from 211 lumbar punctures. J Neurol Sci 306(1–2):82–90CrossRefPubMed

50.

Chang KH, Tseng MY, Ro LS, Lyu RK, Tai YH, Chang HS, Wu YR, Huang CC, Hsu WC, Kuo HC et al (2013) Analyses of haptoglobin level in the cerebrospinal fluid and serum of patients with neuromyelitis optica and multiple sclerosis. Clin Chim Acta Int J Clin Chem 417:26–30CrossRef

Title: Features of anti-aquaporin 4 antibody-seropositive Chinese patients with neuromyelitis optica spectrum optic neuritis
Authors: Hongyang Li
Yanling Wang
Quangang Xu
Aidi Zhang
Huanfen Zhou
Shuo Zhao
Hao Kang
Chunxia Peng
Shanshan Cao
Shihui Wei
Publication date: 01-10-2015
Publisher: Springer Berlin Heidelberg
Published in: Journal of Neurology / Issue 10/2015
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-015-7844-y

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Features of anti-aquaporin 4 antibody-seropositive Chinese patients with neuromyelitis optica spectrum optic neuritis

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 10/2015

Refining the phenotype of inborn errors of metabolism

Genetic landscape remodelling in spinocerebellar ataxias: the influence of next-generation sequencing

A multimodal neuroimaging study of a case of crossed nonfluent/agrammatic primary progressive aphasia

Renal dysfunction is associated with deep cerebral microbleeds but not white matter hyperintensities in patients with acute intracerebral hemorrhage

Rituximab as first-line therapy in neuromyelitis optica: efficiency and tolerability

Relevance of hippocampal integrity for memory outcome after surgical treatment of mesial temporal lobe epilepsy