Advances on the diagnosis and treatment of aquaporin 4 antibody positive neuromyelitis optica spectrum disorders

doi:10.3969/j.issn.1672-6731.2024.05.002

Abstract

Abstract:

Neuromyelitis optica spectrum disorders (NMOSDs) are most common in anti -aquaporin 4 (AQP4) antibody positive NMOSDs, which are characterized by recurrent episodes of optic neuritis and myelitis, etc., and severely reduce the quality of life. In recent years, new insights into the diagnostic techniques, diagonstic markers, and immunotherapy of anti-AQP4 antibody positive NMOSDs have continued to emerge, and here we focus on synthesizing new advances in the diagnostic techniques and diagonstic markers of anti-AQP4 antibody positive NMOSDs and the most recent recommendations for its treatment, in hopes of summarizing to promote the understanding and application of new diagnostic and therapeutic techniques for anti-AQP4 antibody positive NMOSDs in China, and to explore more possible clinical diagnostic and therapeutic approaches.

Key words: Neuromyelitis optica, Aquaporin 4, Immunotherapy, Review

摘要：

视神经脊髓炎谱系疾病（NMOSDs）以抗水通道蛋白4（AQP4）抗体阳性NMOSDs最为多见，主要表现为反复发作的视神经炎和脊髓炎等，严重降低患者生活质量。近年来，对该病的诊断技术、诊断标志物和免疫治疗药物不断有新的认识，本文综述抗AQP4抗体阳性NMOSDs的诊断技术和诊断标志物新进展以及新的治疗药物，以促进对该病的诊断与治疗新技术的理解和应用，探索更多可能的临床诊断与治疗方法。

关键词: 视神经脊髓炎, 水通道蛋白质4, 免疫疗法, 综述

CLC Number:

Hong-jia XU, Ya-qing SHU, Pin WANG, Fan LI, Shun-liang XU, Wei QIU, Xiao-yu MA. Advances on the diagnosis and treatment of aquaporin 4 antibody positive neuromyelitis optica spectrum disorders[J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(5): 308-314.

许鸿嘉, 舒崖清, 王蘋, 李蕃, 许顺良, 邱伟, 马晓宇. 抗水通道蛋白4抗体阳性视神经脊髓炎谱系疾病诊断与治疗进展[J]. 中国现代神经疾病杂志, 2024, 24(5): 308-314.

/ / Recommend / Download Citations

URL: https://journal11.magtechjournal.com/cjcnn/EN/10.3969/j.issn.1672-6731.2024.05.002

https://journal11.magtechjournal.com/cjcnn/EN/Y2024/V24/I5/308

References 34

1	Bennett JL , O'Connor KC , Bar-Or A , Zamvil SS , Hemmer B , Tedder TF , von Büdingen HC , Stuve O , Yeaman MR , Smith TJ , Stadelmann C . B lymphocytes in neuromyelitis optica. Neurol Neuroimmunol Neuroinflamm, 2015, 2: e104. doi: 10.1212/NXI.0000000000000104
2	Neuroimmunology Branch, Chinese Society of Immunology . Diagnosis and treatment guidelines for optic neuromyelitis spectrum diseases in China (2021 edition). Zhongguo Shen Jing Mian Yi Xue He Shen Jing Bing Xue Za Zhi, 2021, 28: 423- 436. URL
	中国免疫学会神经免疫分会. 中国视神经脊髓炎谱系疾病诊断与治疗指南(2021版). 中国神经免疫学和神经病学杂志, 2021, 28: 423- 436. URL
3	Jarius S , Paul F , Aktas O , Asgari N , Dale RC , de Seze J , Franciotta D , Fujihara K , Jacob A , Kim HJ , Kleiter I , Kümpfel T , Levy M , Palace J , Ruprecht K , Saiz A , Trebst C , Weinshenker BG , Wildemann B . MOG encephalomyelitis: international recommendations on diagnosis and antibody testing. J Neuroinflammation, 2018, 15: 134. doi: 10.1186/s12974-018-1144-2
4	Kümpfel T , Giglhuber K , Aktas O , Ayzenberg I , Bellmann-Strobl J , Häußler V , Havla J , Hellwig K , Hümmert MW , Jarius S , Kleiter I , Klotz L , Krumbholz M , Paul F , Ringelstein M , Ruprecht K , Senel M , Stellmann JP , Bergh FT , Trebst C , Tumani H , Warnke C , Wildemann B , Berthele A , Neuromyelitis Optica Study Group (NEMOS) . Update on the diagnosis and treatment of neuromyelitis optica spectrum disorders (NMOSD): revised recommendations of the Neuromyelitis Optica Study Group (NEMOS). Part Ⅱ: attack therapy and long-term management. J Neurol, 2024, 271: 141- 176. doi: 10.1007/s00415-023-11910-z
5	Jarius S , Aktas O , Ayzenberg I , Bellmann-Strobl J , Berthele A , Giglhuber K , Häußler V , Havla J , Hellwig K , Hümmert MW , Kleiter I , Klotz L , Krumbholz M , Kümpfel T , Paul F , Ringelstein M , Ruprecht K , Senel M , Stellmann JP , Bergh FT , Tumani H , Wildemann B , Trebst C , Neuromyelitis Optica Study Group (NEMOS) . Update on the diagnosis and treatment of neuromyelits optica spectrum disorders (NMOSD): revised recommendations of the Neuromyelitis Optica Study Group (NEMOS). Part Ⅰ: diagnosis and differential diagnosis. J Neurol, 2023, 270: 3341- 3368. doi: 10.1007/s00415-023-11634-0
6	Wingerchuk DM , Banwell B , Bennett JL , Cabre P , Carroll W , Chitnis T , de Seze J , Fujihara K , Greenberg B , Jacob A , Jarius S , Lana-Peixoto M , Levy M , Simon JH , Tenembaum S , Traboulsee AL , Waters P , Wellik KE , Weinshenker BG , International Panel for NMO Diagnosis . International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology, 2015, 85: 177- 189. doi: 10.1212/WNL.0000000000001729
7	Chinese Society of Neuroimmunology . Expert consensus on the detection of antibodies associated with autoimmune diseases of the central nervous system 2022. Zhonghua Shen Jing Ke Za Zhi, 2023, 56: 257- 268.
	中华医学会神经病学分会神经免疫学组. 中枢神经系统自身免疫性疾病相关抗体检测专家共识2022. 中华神经科杂志, 2023, 56: 257- 268.
8	Fu Y , Bi J , Yan Y , Sun X , Li K , Kim SY , Han SM , Zhou L , Li R , Huang Q , Wang N , Lin A , Kim HJ , Qiu W . Rapid immunodot AQP4 assay for neuromyelitis optica spectrum disorder. JAMA Neurol, 2023, 80: 1105- 1112. doi: 10.1001/jamaneurol.2023.2974
9	Paul F , Marignier R , Palace J , Arrambide G , Asgari N , Bennett JL , Cree BAC , De Sèze J , Fujihara K , Kim HJ , Hornby R , Huda S , Kissani N , Kleiter I , Kuwabara S , Lana-Peixoto M , Law L , Leite MI , Pandit L , Pittock SJ , Quan C , Ramanathan S , Rotstein D , Saiz A , Sato DK , Vaknin-Dembinsky A . International Delphi consensus on the management of AQP4-IgG+NMOSD: recommendations for eculizumab, inebilizumab, and satralizumab. Neurol Neuroimmunol Neuroinflamm, 2023, 10: e200124. doi: 10.1212/NXI.0000000000200124
10	Aktas O , Smith MA , Rees WA , Bennett JL , She D , Katz E , Cree BAC , N-MOmentum Scientific Group and the N-MOmentum Study Investigators . Serum glial fibrillary acidic protein: aneuromyelitis optica spectrum disorder biomarker. Ann Neurol, 2021, 89: 895- 910. doi: 10.1002/ana.26067
11	Schindler P , Grittner U , Oechtering J , Leppert D , Siebert N , Duchow AS , Oertel FC , Asseyer S , Kuchling J , Zimmermann HG , Brandt AU , Benkert P , Reindl M , Jarius S , Paul F , Bellmann-Strobl J , Kuhle J , Ruprecht K . Serum GFAP and NfL as disease severity and prognostic biomarkers in patients with aquaporin-4 antibody-positive neuromyelitis optica spectrum disorder. J Neuroinflammation, 2021, 18: 105. doi: 10.1186/s12974-021-02138-7
12	Aktas O , Hartung HP , Smith MA , Rees WA , Paul F , Marignier R , Bennett JL , Kim HJ , Weinshenker BG , Pittock SJ , Wingerchuk DM , Cutter G , She D , Gunsior M , Cimbora D , Katz E , Cree BA , N-MOmentum Study Investigators . Serum-neurofilament light chain levels at attack predict post attack disability worsening and are mitigated by inebilizumab: analysis of four potential biomarkers in neuromyelitis optica spectrum disorder. J Neurol Neurosurg Psychiatry, 2023, 94: 757- 768. doi: 10.1136/jnnp-2022-330412
13	Nie T , Blair HA . Inebilizumab: a review in neuromyelitis optica spectrum disorder. CNS Drugs, 2022, 36: 1133- 1141. doi: 10.1007/s40263-022-00949-7
14	Pittock SJ , Berthele A , Fujihara K , Kim HJ , Levy M , Palace J , Nakashima I , Terzi M , Totolyan N , Viswanathan S , Wang KC , Pace A , Fujita KP , Armstrong R , Wingerchuk DM . Eculizumab in aquaporin-4-positive neuromyelitis optica spectrum disorder. N Engl J Med, 2019, 381: 614- 625. doi: 10.1056/NEJMoa1900866
15	Wingerchuk DM , Fujihara K , Palace J , Berthele A , Levy M , Kim HJ , Nakashima I , Oreja-Guevara C , Wang KC , Miller L , Shang S , Sabatella G , Yountz M , Pittock SJ , PREVENT Study Group . Long-term safety and efficacy of eculizumab in aquaporin-4 IgG-positive NMOSD. Ann Neurol, 2021, 89: 1088- 1098. doi: 10.1002/ana.26049
16	Palace J , Wingerchuk DM , Fujihara K , Berthele A , Oreja-Guevara C , Kim HJ , Nakashima I , Levy M , Terzi M , Totolyan N , Viswanathan S , Wang KC , Pace A , Yountz M , Miller L , Armstrong R , Pittock S , PREVENT Study Group . Benefits of eculizumab in AQP4+ neuromyelitis optica spectrum disorder: subgroup analyses of the randomized controlled phase 3 PREVENT trial. Mult Scler Relat Disord, 2021, 47: 102641. doi: 10.1016/j.msard.2020.102641
17	Sen S , Tuncer A , Terzi M , Bunul SD , Ozen-Acar P , Altunrende B , Ozakbas S , Tutuncu M , Uygunoglu U , Akman-Demir G , Karabudak R , Efendi H , Siva A . Severe disease reactivation in seropositive neuromyelitis optica spectrum disorders patients after stopping eculizumab treatment. Mult Scler Relat Disord, 2023, 79: 104949. doi: 10.1016/j.msard.2023.104949
18	Cree BAC , Bennett JL , Kim HJ , Weinshenker BG , Pittock SJ , Wingerchuk DM , Fujihara K , Paul F , Cutter GR , Marignier R , Green AJ , Aktas O , Hartung HP , Lublin FD , Drappa J , Barron G , Madani S , Ratchford JN , She D , Cimbora D , Katz E , N-MOmentum Study Investigators . Inebilizumab for the treatment of neuromyelitis optica spectrum disorder (N-MOmentum): a double-blind, randomised placebo-controlled phase 2/3 trial. Lancet, 2019, 394: 1352- 1363. doi: 10.1016/S0140-6736(19)31817-3
19	Rensel M , Zabeti A , Mealy MA , Cimbora D , She D , Drappa J , Katz E . Long-term efficacy and safety of inebilizumab in neuromyelitis optica spectrum disorder: analysis of aquaporin-4-immunoglobulin G-seropositive participants taking inebilizumab for ≥ 4 years in the N-MOmentum trial. Mult Scler, 2022, 28: 925- 932. doi: 10.1177/13524585211047223
20	Howard JF Jr , Utsugisawa K , Benatar M , Murai H , Barohn RJ , Illa I , Jacob S , Vissing J , Burns TM , Kissel JT , Muppidi S , Nowak RJ , O'Brien F , Wang JJ , Mantegazza R , REGAIN Study Group . Safety and efficacy of eculizumab in anti-acetylcholine receptor antibody-positive refractory generalised myasthenia gravis (REGAIN): a phase 3, randomised, double-blind, placebo-controlled, multicentre study. Lancet Neurol, 2017, 16: 976- 986. doi: 10.1016/S1474-4422(17)30369-1
21	Kim HJ , Nakashima I , Viswanathan S , Wang KC , Shang S , Miller L , Yountz M , Wingerchuk DM , Pittock SJ , Levy M , Berthele A , Totolyan N , Palace J , Barnett MH , Fujihara K , PREVENT Study Group . Eculizumab in Asian patients with anti-aquaporin-IgG-positive neuromyelitis optica spectrum disorder: a subgroup analysis from the randomized phase 3 PREVENT trial and its open-label extension. Mult Scler Relat Disord, 2021, 50: 102849. doi: 10.1016/j.msard.2021.102849
22	Nakashima I , Nakahara J , Yokote H , Manabe Y , Okamura K , Hasegawa K , Fujihara K . Long-term safety and effectiveness of eculizumab in patients with aquaporin-4 antibody-positive neuromyelitis optica spectrum disorder: a 2-year interim analysis of post-marketing surveillance in Japan. Ther Adv Neurol Disord, 2023, 16: 1- 13.
23	Agius MA , Klodowska-Duda G , Maciejowski M , Potemkowski A , Li J , Patra K , Wesley J , Madani S , Barron G , Katz E , Flor A . Safety and tolerability of inebilizumab (MEDI-551), an anti-CD19 monoclonal antibody, in patients with relapsing forms of multiple sclerosis: results from a phase 1 randomised, placebo-controlled, escalating intravenous and subcutaneous dose study. Mult Scler, 2019, 25: 235- 245. doi: 10.1177/1352458517740641
24	Flanagan EP , Levy M , Katz E , Cimbora D , Drappa J , Mealy MA , She D , Cree BAC . Inebilizumab for treatment of neuromyelitis optica spectrum disorder in patients with prior rituximab use from the N-MOmentum Study. Mult Scler Relat Disord, 2022, 57: 103352. doi: 10.1016/j.msard.2021.103352
25	Bennett JL , Aktas O , Rees WA , Smith MA , Gunsior M , Yan L , She D , Cimbora D , Pittock SJ , Weinshenker BG , Paul F , Marignier R , Wingerchuk D , Cutter G , Green A , Hartung HP , Kim HJ , Fujihara K , Levy M , Katz E , Cree BAC , N-MOmentum Study Investigators . Association between B-cell depletion and attack risk in neuromyelitis optica spectrum disorder: an exploratory analysis from N-MOmentum, a double-blind, randomised, placebo-controlled, multicentre phase 2/3 trial. EBioMedicine, 2022, 86: 104321. doi: 10.1016/j.ebiom.2022.104321
26	Kim HJ , Aktas O , Patterson KR , Korff S , Kunchok A , Bennett JL , Weinshenker BG , Paul F , Hartung HP , Cimbora D , Smith MA , Mittereder N , Rees WA , She D , Cree BAC . Inebilizumab reduces neuromyelitis optica spectrum disorder risk independent of FCGR3A polymorphism. Ann Clin Transl Neurol, 2023, 10: 2413- 2420. doi: 10.1002/acn3.51911
27	Igawa T , Ishii S , Tachibana T , Maeda A , Higuchi Y , Shimaoka S , Moriyama C , Watanabe T , Takubo R , Doi Y , Wakabayashi T , Hayasaka A , Kadono S , Miyazaki T , Haraya K , Sekimori Y , Kojima T , Nabuchi Y , Aso Y , Kawabe Y , Hattori K . Antibody recycling by engineered pH-dependent antigen binding improves the duration of antigen neutralization. Nat Biotechnol, 2010, 28: 1203- 1207. doi: 10.1038/nbt.1691
28	Yamamura T , Kleiter I , Fujihara K , Palace J , Greenberg B , Zakrzewska-Pniewska B , Patti F , Tsai CP , Saiz A , Yamazaki H , Kawata Y , Wright P , De Seze J . Trial of satralizumab in neuromyelitis optica spectrum disorder. N Engl J Med, 2019, 381: 2114- 2124. doi: 10.1056/NEJMoa1901747
29	Traboulsee A , Greenberg BM , Bennett JL , Szczechowski L , Fox E , Shkrobot S , Yamamura T , Terada Y , Kawata Y , Wright P , Gianella-Borradori A , Garren H , Weinshenker BG . Safety and efficacy of satralizumab monotherapy in neuromyelitis optica spectrum disorder: a randomised, double-blind, multicentre, placebo-controlled phase 3 trial. Lancet Neurol, 2020, 19: 402- 412. doi: 10.1016/S1474-4422(20)30078-8
30	Kleiter I , Traboulsee A , Palace J , Yamamura T , Fujihara K , Saiz A , Javed A , Mayes D , Büdingen HV , Klingelschmitt G , Stokmaier D , Bennett JL . Long-term efficacy of satralizumab in AQP4-IgG-seropositive neuromyelitis optica spectrum disorder from SAkuraSky and SAkuraStar. Neurol Neuroimmunol Neuroinflamm, 2022, 10: e200071.
31	Lennon-Chrimes S , Baumann HS , Klingelschmitt G , Kou X , Anania VG , Ito H , von Budingen HC . Characterisation of the PK and PD of satralizumab, a recycling antibody, to Support Q4W dosing in patients with NMOSD. Neurology, 2020, 94
32	Yamamura T , Weinshenker B , Yeaman MR , De Seze J , Patti F , Lobo P , von Büdingen HC , Kou X , Weber K , Greenberg B . Long-term safety of satralizumab in neuromyelitis optica spectrum disorder (NMOSD) from SAkuraSky and SAkuraStar. Mult Scler Relat Disord, 2022, 66: 104025. doi: 10.1016/j.msard.2022.104025
33	Vu T , Ortiz S , Katsuno M , Annane D , Mantegazza R , Beasley KN , Aguzzi R , Howard JF Jr . Ravulizumab pharmacokinetics and pharmacodynamics in patients with generalized myasthenia gravis. J Neurol, 2023, 270: 3129- 3137. doi: 10.1007/s00415-023-11617-1
34	Pittock SJ , Barnett M , Bennett JL , Berthele A , de Sèze J , Levy M , Nakashima I , Oreja-Guevara C , Palace J , Paul F , Pozzilli C , Yountz M , Allen K , Mashhoon Y , Kim HJ . Ravulizumab in aquaporin-4-positive neuromyelitis optica spectrum disorder. Ann Neurol, 2023, 93: 1053- 1068. doi: 10.1002/ana.26626

[1]	Zhi-yong TONG. Intracranial aneurysms and cerebral revascularization [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(8): 595-598.
[2]	Zhi-yong TONG. History of cerebral revascularization [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(8): 599-605.
[3]	Ling-ji JIN, Jun-wen HU, Yin LI, Lin WANG. Intracranial-intracranial bypass for the treatment of complex intracranial aneurysms: technical advances and surgical experience [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(8): 606-612.
[4]	Pei-xi LIU, Yuan SHI, Wei ZHU. Application of whole-region cerebral vascular bypass for intracranial aneurysms treatment in the flow diversion era [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(8): 613-618.
[5]	Feng ZHANG, Fan-gang MENG. Research progress of subthalamic nucleus deep brain stimulation in treatment of autonomic nerve dysfunction in Parkinson's disease [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(7): 510-515.
[6]	Gui-zhi WU, Hong TIAN. Clinical research progress of deep brain stimulation for Meige's syndrome [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(7): 516-521.
[7]	Fan-gang MENG, Jian-guo ZHANG. Application of retroauricular bone grinding groove technology in deep brain stimulation [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(7): 522-524.
[8]	Lin CHEN, Hua PAN. Electrophysiological diagnosis of functional tremor [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(7): 573-578.
[9]	Jun-ji WEI, Jian-bo CHANG. Promoting the concept of neurosurgical critical care in primary hospitals [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(6): 403-406.
[10]	Rui ZHANG, Yong-li TAO, Chen-yang JIANG, Kai LIU, Yu-ming XU, Bo SONG. Observation of the efficacy of ofatumumab in the treatment of neuromyelitis optica spectrum disorders [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(6): 491-496.
[11]	Ruo-lin SHI, Xiu-jie GAO, Jia-ning CUI, Yan SHAO, Lu-shuang XIE, Yi LIU. Advance on association between 5-hydroxytryptamine and non-motor symptoms in Parkinson's disease [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(6): 497-501.
[12]	Hai-feng LI. Glucocorticoids remain the basis for treatment of myasthenia gravis in the era of targeted therapies [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(5): 295-307.
[13]	Yu HUANG, Jin-chi LIAO, Ya-qing SHU. Progress on sleep disorders in anti-N-methyl-D-aspartate receptor encephalitis [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(5): 315-319.
[14]	Cai-yun LIU, Tao JIN. Immunotherapeutic potential of dendritic cells in multiple sclerosis [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(5): 320-330.
[15]	Hong-ling QIN, Qi-hui LI, Yi LU, Wei QIU, Ya-qing SHU. Clinical analysis and literature review of anti-contactin-associated protein 2 antibody-associated encephalitis [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2024, 24(5): 340-345.

Please choose a citation manager

Content to export