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Abstract

Objective:

To evaluate clinical features among patients with neuromyelitis optica spectrum disorders (NMOSD) who have myelin oligodendrocyte glycoprotein (MOG) antibodies, aquaporin-4 (AQP4) antibodies, or seronegativity for both antibodies.

Methods:

Sera from patients diagnosed with NMOSD in 1 of 3 centers (2 sites in Brazil and 1 site in Japan) were tested for MOG and AQP4 antibodies using cell-based assays with live transfected cells.

Results:

Among the 215 patients with NMOSD, 7.4% (16/215) were positive for MOG antibodies and 64.7% (139/215) were positive for AQP4 antibodies. No patients were positive for both antibodies. Patients with MOG antibodies represented 21.1% (16/76) of the patients negative for AQP4 antibodies. Compared with patients with AQP4 antibodies or patients who were seronegative, patients with MOG antibodies were more frequently male, had a more restricted phenotype (optic nerve more than spinal cord), more frequently had bilateral simultaneous optic neuritis, more often had a single attack, had spinal cord lesions distributed in the lower portion of the spinal cord, and usually demonstrated better functional recovery after an attack.

Conclusions:

Patients with NMOSD with MOG antibodies have distinct clinical features, fewer attacks, and better recovery than patients with AQP4 antibodies or patients seronegative for both antibodies.

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Supplementary Material

File (466.pdf)
File (e-methods.docx)
File (kazutoshi_474.pdf)
File (tables_e-1-3.docx)

REFERENCES

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Wingerchuk DM, Hogancamp WF, O'Brien PC, Weinshenker BG. The clinical course of neuromyelitis optica (Devic's syndrome). Neurology 1999;53:1107–1114.
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Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG. The spectrum of neuromyelitis optica. Lancet Neurol 2007;6:805–815.
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Mader S, Gredler V, Schanda K, et al. Complement activating antibodies to myelin oligodendrocyte glycoprotein in neuromyelitis optica and related disorders. J Neuroinflammation 2011;8:184.
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Letters to the Editor
12 May 2014
Response to: Anti-MOG+ ON: a mystery yet unknown
Douglas K. Sato, Neurologist
Douglas Kazutoshi Sato, Sendai, Japan; Dagoberto Callegaro, Sao Paulo, Brazil; Marco Aurelio Lana-Peixoto, Belo Horizonte, Brazil; Ichiro Nakashima, Sendai, Japan; Kazuo Fujihara, Sendai, Japa

We thank Hu et al. for their comments. We found that some patients with recurrent and/or bilateral simultaneous optic neuritis (ON) had antibodies against myelin-oligodendrocyte glycoprotein (MOG). [1] Anti-MOG+ ON cases have also been reported in other studies using cell-based assays to detect conformation-sensitive anti-MOG antibodies, [2 4] confirming the presence of anti-MOG+ ON in distinct cohorts. The patients' referral system--established for each center--may influence the study cohort, which constitutes a potential study limitation. Therefore, multicenter studies including different countries like our study are less vulnerable to this bias than single-center or country-based studies. Expanded Disability Status Scale (EDSS) is calculated by assessments of functional systems, but it may have some limitations to represent visual deficits, especially in cases with overwhelming walking difficulty.5 We have analyzed not only the EDSS but also the visual acuity of each patient with ON, and anti-MOG+ patients had less visual impairment after treatment, suggesting a better prognosis compared to patients with anti-aquaporin-4 antibodies. Further prospective studies may confirm that anti-MOG+ ON has a lower number of relapses and risk of permanent visual loss. Magnetic resonance imaging and optical coherence tomography studies in anti-MOG+ ON cases may indicate additional clinical and prognostic features.

1. Sato DK, Callegaro D, Lana-Peixoto MA, et al. Distinction between MOG antibody-positive and AQP4 antibody-positive NMO spectrum disorders. Neurology 2014;82:474-481.

2. Mader S, Gredler V, Schanda K, et al. Complement activating antibodies to myelin oligodendrocyte glycoprotein in neuromyelitis optica and related disorders. J Neuroinflammation 2011;8:184.

3. Reindl M, Di Pauli F, Rostasy K, Berger T. The spectrum of MOG autoantibody-associated demyelinating diseases. Nat Rev Neurol 2013;9:455- 461.

4. Tanaka M, Tanaka K. Anti-MOG antibodies in adult patients with demyelinating disorders of the central nervous system. J Neuroimmunol 2014;270:98-99.

5. Garcia-Martin E, Rodriguez-Mena D, Herrero R, et al. Neuro- ophthalmologic evaluation, quality of life, and functional disability in patients with MS. Neurology 2013;81:76-83.

For disclosures, contact the editorial office at [email protected].

11 March 2014
Anti-MOG+ ON: a mystery yet unknown
Xueqiang Hu, Doctor
Zhifeng Mao, Zhengqi Lu, Xueqiang Hu

Sato et al. assessed the differences among patients with neuromyelitis optica spectrum disorders (NMOSD) who have myelin oligodendrocyte glycoprotein (MOG) antibodies, aquaporin-4 (AQP4) antibodies, or seronegativity for both antibodies. [1] They observed that optic neuritis (ON) was more frequent in anti-MOG+ patients. This conflicts with another recent study in which Anti-MOG+ ON was not reported, while simultaneous/sequential ON and myelitis were seen more frequently. [2] However, this estimation may not be accurate due to different race and adequate sample sizes. The 5-year conversion rate from ON to NMO is approximately 12.5% and the interval conversion is usually more than 2 years and even longer in anti-AQP4 patients. [3] Six anti-MOG+ NMO patients with relapse were reported after long-term follow up. [2,4] The potential second attack in anti-MOG+ patients may be underestimated because of limited follow-up. Although anti-MOG+ patients tend to have less relapse, knowing this potential relapse risk is important. ON assessment with the Expanded Disability Status Scale might be imprecise as visual loss contributed little to the EDSS score. Subgroup analysis like anti- MOG+ ON vs. anti-AQP4+ ON using visual acuity measures may be necessary for differential consideration.

1.Sato DK, Callegaro D, Lana-Peixoto MA, et al. Distinction between MOG antibody-positive and AQP4 antibody-positive NMO spectrum disorders. Neurology 2014;82:474-481.

2.Kitley J, Waters P, Woodhall M, et al. Neuromyelitis Optica Spectrum Disorders With Aquaporin-4 and Myelin-Oligodendrocyte Glycoprotein Antibodies: A Comparative Study. JAMA Neurol 2014;Jan 13.

3.Pirko I, Blauwet LA, Lesnick TG, Weinshenker BG. The natural history of recurrent optic neuritis. Arch Neurol 2004;61:1401-1405.

4.Mader S, Gredler V, Schanda K, et al. Complement activating antibodies to myelin oligodendrocyte glycoprotein in neuromyelitis optica and related disorders. J Neuroinflammation 2011;8:184.

For disclosures, contact the editorial office at [email protected].

4 February 2014
Response to "Existence of anti-AQP4+ and anti-MOG+ neuromyelitis optica with severe recurrent optic neuritis"
Douglas K. Sato, Neurologist
Douglas Kazutoshi Sato, Sendai, Japan; Toshiyuki Takahashi, Sendai, Japan; Patrick J. Waters, Oxford, UK; Kazuo Fujihara, Sendai, Japan
We thank Kezuka et al. for sharing their experience with two neuromyelitis optica patients that were likely to be positive to both AQP4-antibodies and MOG-antibodies. The clinical features of these two patients were compatible with AQP4-antibody seropositive NMO as [1, 2] both were middle-aged females with severe attacks of optic neuritis and longitudinally extensive myelitis. The patients with AQP4-antibodies were not expected to have a less severe disease course as we found in our cases with MOG-antibodies alone. [3] Similar to our results, Kitley et al. [4] reported NMO spectrum disorder patients with AQP4-antibodies (n = 20) or MOG-antibodies (n = 9) tested at Oxford University with no double-positive cases. However, this does not exclude the possibility of double-positive cases. Their and our patients with MOG-antibodies have similarities. Currently, it is not clear if differences on the cell-based assays (CBA) developed by each center could yield different results. The positivity for both antibodies, instead of nonspecific binding, might be clarified by testing MOG-antibodies in pre-adsorbed sera for AQP4 and vice-versa. Dr Kezuka also reported that 4 of 6 patients (66.7%) may have had false-positive results by ELISA for MOG-antibodies, suggesting that ELISA failed to discriminate conformational-specific MOG-antibodies. [5]

1. Wingerchuk DM, Lennon VA, Lucchinetti CF, Pittock SJ, Weinshenker BG. The spectrum of neuromyelitis optica. Lancet Neurol 2007;6:805-815.

2. Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG. Revised diagnostic criteria for neuromyelitis optica. Neurology 2006;66:1485-1489.

3. Sato DK, Callegaro D, Lana-Peixoto MA, et al. Distinction between MOG antibody-positive and AQP4 antibody-positive NMO spectrum disorders. Neurology 2014;82:doi 10.1212/wnl.0000000000000101.

4. Kitley J, Waters P, Woodhall M, et al. Neuromyelitis Optica Spectrum Disorders With Aquaporin-4 and Myelin-Oligodendrocyte Glycoprotein Antibodies. JAMA Neurol 2014:doi 10.1001/jamaneurol.2013.5857.

5. O'Connor KC, McLaughlin KA, De Jager PL, et al. Self-antigen tetramers discriminate between myelin autoantibodies to native or denatured protein. Nature Medicine 2007;13:211-217.

For disclosures, contact the editorial office at [email protected].

28 January 2014
Existence of anti-AQP4+ and anti-MOG+ neuromyelitis optica with severe recurrent optic neuritis
Takeshi Kezuka, Associate Professor
Takeshi Kezuka, Tokyo, Japan; Keiko Tanaka, Ishikawa, Japan; Yoshimishi Matsunaga, Tokyo, Japan; Hiroshi Goto, Tokyo, Japan

Sato et al. reported results from Japanese and Brazilian patients with neuromyelitis optica (NMO) evaluated for the presence of serum antibodies targeting aquaporin-4 (AQP4) and myelin oligodendrocyte glycoprotein (MOG). [1] In their study, none of the patients was positive for both anti-AQP4 and anti-MOG antibodies. However, in our previously reported study, 6 of 23 (26%) patients were seropositive for both anti-NMO and anti-MOG antibodies. [2] Editorialists Weinshenker and Wingerchuk [3] suggested that the difference in methodology of detection (ELISA in our study versus cell-based assay in Sato et al.???s study) may contribute to the discrepancy. However, in recent cell- based assay using full length human MOG cDNA expressing HEK cells, we found two patients who were anti-AQP4+ and anti-MOG+. Both patients were middle-aged women with NMO and both had repeated ocular attacks; 4 times in one and 8 times in the other. Both had bilateral optic neuritis with longitudinally extensive myelitis. The clinical characteristics of these two patients are recurrent optic neuritis and poor visual outcome despite treatment, which differs from the clinical profile reported by Sato et al. [1] Our results indicate that anti-AQP4+ and anti-MOG+ NMO does exist, irrespective of the methodology of anti-MOG antibodies detection, and this form of NMO often has severe ocular disease.

1. Sato DK, Callegaro D, Lana-Peixoto MA, et al. Distinction between MOG antibody-positive and AQP4 antibody positive NMO spectrum disorders. Neurology 2014;82:WNL.0000000000000101v1-101212000.

2. Kezuka T, Usui Y, Yamakawa N, et al. Relationship between NMO-antibody and anti-MOG antibody in optic neuritis. J Neuro-ophthalmology 2012;32: 107-110.

3. Weinshenker BG, Wingerchuk DM. The two faces of neuromyelitis optica. Neurology 2014;82:XXX-XXX.

For disclosures, contact the editorial office at [email protected].

Information & Authors

Information

Published In

Neurology®
Volume 82Number 6February 11, 2014
Pages: 474-481
PubMed: 24415568

Publication History

Received: June 9, 2013
Accepted: September 23, 2013
Published online: January 10, 2014
Published in print: February 11, 2014

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Disclosure

D. Sato receives scholarship from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan and has received research support from Ichiro Kanehara Foundation. D. Callegaro and M. Lana-Peixoto report no disclosures. P. Waters is a named inventor and has received royalties for antibody assays, and has received a speaker honorarium from Biogen Idec Japan. F. Jorge and T. Takahashi report no disclosures. I. Nakashima has received funding for travel and received speaker honoraria from Bayer Schering Pharma and Biogen Idec and has received research funding from Mitsubishi Chemical Medience Corporation and the Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Technology of Japan. S. Apostolos-Pereira, N. Talim, R. Simm, and A. Lino report no disclosures. T. Misu has received speaker honoraria from Bayer Schering Pharma, Biogen Idec Japan, Mitsubishi Tanabe Pharma Corporation, Asahi Kasei Medical Co., and Astellas Pharma Inc., and has received research support from Bayer Schering Pharma, Biogen Idec Japan, Asahi Kasei Kuraray Medical Co., The Chemo-Sero-Therapeutic Research Institute, Teva Pharmaceutical K.K., Mitsubishi Tanabe Pharma Corporation, Teijin Pharma, and Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Technology, and the Ministry of Health, Labor and Welfare of Japan. M. Leite is supported by NHS National Specialised Commissioning Group for Neuromyelitis Optica, UK, and by NIHR Oxford Biomedical Research Centre, and has received speaking honoraria from Biogen Idec and travel grants from Novartis. M. Aoki reports no disclosures. K. Fujihara serves on scientific advisory boards for Bayer Schering Pharma, Biogen Idec, Mitsubishi Tanabe Pharma Corporation, Novartis Pharma, Chugai Pharmaceutical, Ono Pharmaceutical, Nihon Pharmaceutical, Merck Serono, Alexion Pharmaceuticals, Medimmune and Medical Review; has received funding for travel and speaker honoraria from Bayer Schering Pharma, Biogen Idec, Eisai Inc., Mitsubishi Tanabe Pharma Corporation, Novartis Pharma, Astellas Pharma Inc., Takeda Pharmaceutical Company Limited, Asahi Kasei Medical Co., Daiichi Sankyo, and Nihon Pharmaceutical; serves as an editorial board member of Clinical and Experimental Neuroimmunology (2009–present) and an advisory board member of Sri Lanka Journal of Neurology; has received research support from Bayer Schering Pharma, Biogen Idec Japan, Asahi Kasei Medical, The Chemo-Sero-Therapeutic Research Institute, Teva Pharmaceutical, Mitsubishi Tanabe Pharma, Teijin Pharma, Chugai Pharmaceutical, Ono Pharmaceutical, Nihon Pharmaceutical, and Genzyme Japan; and is funded as the secondary investigator (22229008, 2010–2015) by the Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Technology of Japan and as the secondary investigator by the Grants-in-Aid for Scientific Research from the Ministry of Health, Welfare and Labor of Japan (2010–present). Go to Neurology.org for full disclosures.

Study Funding

Supported by KAKENHI (22229008) of The Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan, and by the Health and Labour Sciences Research Grant on Intractable Diseases (Neuroimmunological Diseases) from the Ministry of Health, Labour and Welfare of Japan.

Authors

Affiliations & Disclosures

Douglas Kazutoshi Sato, MD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
(1) Ministry of Education, Culture, Sports, Science & Technology (MEXT) in Japan, Japanese Government Scholarship Program, 4 years (2010 - 2014)
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
(1) Ichiro Kanehara Foundation
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
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1.
NONE
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1.
NONE
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NONE
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Dagoberto Callegaro, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
(1) Biogen, (2) Novartis
Gifts:
1.
(1) Biogen, (2) Novartis
Funding for Travel or Speaker Honoraria:
1.
(1) Biogen,(2) Novartis
Editorial Boards:
1.
BCTRIMS
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
(1) Biogen, (2) Novartis
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
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NONE
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NONE
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1.
NONE
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Marco Aurelio Lana-Peixoto, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
(1) Advisory board of Gilenya (Novartis) in Brazil
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Funding for travel from Novartis to attend ECTRIMS 2012 in Lyon, France
Editorial Boards:
1.
(1)Arquivos de Neuro-Psiquiatria - Member of the Advisory Editorial Board
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Patrick J. Waters, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Speaker honorarium from Biogen Idec Japan
Editorial Boards:
1.
Frontiers in molecular innate immunity, Review editor, 1 yr
Patents:
1.
Assays for the detection of antibodies to lgi1, Caspr2 and tag-1.
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Frederico M. de Haidar Jorge, MD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Toshiyuki Takahashi, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Ichiro Nakashima, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
Served on the scientific advisory boards for Biogen Idec Japan (2012-2013); Novartis Pharma (2013).
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Recieved funding for a trip and speaks from Bayer Yakuhin Ltd (1999-2012); Biogen Idec Japan (2008-2013); Tanabe Mitsubishi (2012-2013); Novartis Pharma (2012-2013).
Editorial Boards:
1.
Serve as an editorial board member of Multiple Sclerosis International(2010-present).
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
Received grant support from Mitsubishi Chemical Medience Corporation (2012-2013).
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Samira Luisa Apostolos-Pereira, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
(1) Bayer, advisory board, 2011, (2) Biogen Idec, advisory board, 2011
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Natalia Talim
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Renata Faria Simm, MD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Angelina Maria Martins Lino, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
participation in trials of Sanofi-Aventis and Novartis
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
Arquivos de Neuropsiquiatria
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Tatsuro Misu, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Dr. Misu has received speaker honoraria from Bayer Schering Pharma, Biogen Idec., and Mitsubishi Pharma.
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
Dr. Misu has received research support from Bayer Schering Pharma, Biogen Idec Japan, Asahi Kasei Kuraray Medical Co., The Chemo-Sero-Therapeutic Research Institute, Teva Pharmaceutical K.K., Mitsubishi Tanabe Pharma Corporation, Teijin Pharma, and Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Technology, and the Ministry of Health, Labor and Welfare of Japan.
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Maria Isabel Leite, MD, DPhil
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
Dr Leite is supported by NHS National Specialised Commissioning Group for Neuromyelitis optica, UK, and by NIHR Oxford Biomedical Research Centre, and has received speaking honoraria from Biogen Idec and travel and educational grants from Biogen Idec and UK.
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Masashi Aoki, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
NONE
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
NONE
Editorial Boards:
1.
NONE
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
NONE
Research Support, Government Entities:
1.
NONE
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
Masashi Aoki has received research grants, Research on Nervous and Mental disorders, Research on Measures for Intractable Diseases, Research on Psychiatric and Neurological Diseases and Mental Health from the Japanese Ministry of Health Labor and Welfare, Grants-in-Aids for Scientific Research, an Intramural Research Grant for Neurological Psychiatric Disorders from NCNP and Grants-in-Aids for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science and Technology.
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE
Kazuo Fujihara, MD, PhD
From the Departments of Neurology (D.K.S., T.T., I.N., M.A.) and Multiple Sclerosis Therapeutics (T.M., K.F.), Tohoku University Graduate School of Medicine, Sendai, Japan; Department of Neurology (D.C., F.M.d.H.J., S.L.A.-P., R.F.S., A.M.M.L.), Faculty of Medicine, University of São Paulo, Brazil; CIEM MS Research Center (M.A.L.-P., N.T.), Federal University of Minas Gerais Medical School, Belo Horizonte, Brazil; Neuroimmunology Group (P.J.W., M.I.L.), Nuffield Department of Clinical Neurosciences, Oxford University, UK.
Disclosure
Scientific Advisory Boards:
1.
Serves on scientific advisory boards for Bayer Schering Pharma, Biogen Idec, Mitsubishi Tanabe Pharma Corporation, Novartis Pharma, Chugai Pharmaceutical, Ono Pharmaceutical, Nihon Pharmaceutical, Merck Serono, Alexion Pharmaceuticals, Medimmune and Medical Review.
Gifts:
1.
NONE
Funding for Travel or Speaker Honoraria:
1.
has received funding for travel and speaker honoraria from Bayer Schering Pharma, Biogen Idec, Eisai Inc., Mitsubishi Tanabe Pharma Corporation, Novartis Pharma, Astellas Pharma Inc., Takeda Pharmaceutical Company Limited, Asahi Kasei Medical Co., Daiichi Sankyo, and Nihon Pharmaceutical
Editorial Boards:
1.
Serve as an editorial board member of Clinical and Experimental Neuroimmunology (2009-present) and a advisory board member of Sri Lanka journal of Neurology.
Patents:
1.
NONE
Publishing Royalties:
1.
NONE
Employment, Commercial Entity:
1.
NONE
Consultancies:
1.
NONE
Speakers' Bureaus:
1.
NONE
Other Activities:
1.
NONE
Clinical Procedures or Imaging Studies:
1.
NONE
Research Support, Commercial Entities:
1.
has received research support from Bayer Schering Pharma, Biogen Idec Japan, Asahi Kasei Medical, The Chemo-Sero-Therapeutic Research Institute, Teva Pharmaceutical, Mitsubishi Tanabe Pharma, Teijin Pharma, Chugai Pharmaceutical,Ono Pharmaceutical, Nihon Pharmaceutical, and Genzyme Japan.
Research Support, Government Entities:
1.
Funded as the secondary investigator (#22229008, 2010-2015) by the Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Technology of Japan and as the secondary investigator by the Grants-in-Aid for Scientific Research from theMinistry of Health, Welfre and Labor of Japan (2010-present).
Research Support, Academic Entities:
1.
NONE
Research Support, Foundations and Societies:
1.
NONE
Stock/stock Options/board of Directors Compensation:
1.
NONE
License Fee Payments, Technology or Inventions:
1.
NONE
Royalty Payments, Technology or Inventions:
1.
NONE
Stock/stock Options, Research Sponsor:
1.
NONE
Stock/stock Options, Medical Equipment & Materials:
1.
NONE
Legal Proceedings:
1.
NONE

Notes

Correspondence to Dr. Fujihara: [email protected]
Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

Author Contributions

Study design and conceptualization: D.K. Sato, I. Nakashima, A.M.M. Lino, D. Callegaro, and K. Fujihara. Drafting of manuscript: D.K. Sato, T. Takahashi, I. Nakashima, P.J. Waters, M.I. Leite, and K. Fujihara. Acquisition, analysis, and interpretation of data: D.K. Sato, F.M.d.H. Jorge, S.L. Apostolos-Pereira, N. Talim, T. Takahashi, P.J. Waters, I. Nakashima, D. Callegaro, and M.A. Lana-Peixoto. Statistical analysis: D.K. Sato, T. Takahashi, and I. Nakashima. Critical revision of the manuscript: D.K. Sato, P.J. Waters, M.I. Leite, I. Nakashima, T. Misu, T. Takahashi, R.F. Simm, A.M.M. Lino, K. Fujihara, and M. Aoki.

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