Interpret of international Delphi consensus on the management of aquaporin-4 immunoglobulin G seropositive neuromyelitis optica spectrum disorder_Chinese Journal of Ocular Fundus Diseases

Authors：

Li Yuyu , Wei Shihui ,  Zhou Huanfen

Senior Department of Ophthalmology, The Third Medical Center of Chinese PLA General Hospital & Chinese PLA Medical School, Beijing 100853, China;

Corresponding author：

Zhou Huanfen, Email: zhouzhoueye@163.com

Keywords：

Neuromyelitis optica spectrum disorder; Eculizumab; Inebilizumab; Satralizumab; Consensus interpretation

DOI：

10.3760/cma.j.cn511434-20230621-00281

Video：

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Abstract Full text Figures/Tables Video References Cited by

Neuromyelitis optica spectrum disorder (NMOSD) is a rare debilitating autoimmune disease of the central nervous system. Three monoclonal antibodies were recently approved as maintenance therapies for aquaporin-4 immunoglobulin G (AQP4-IgG) seropositive NMOSD (eculizumab, inebilizumab, and satralizumab). Neurol Neuroimmunol Neuroinflamm published international Delphi consensus on the management of AQP4-IgG+ NMOSD in May 31, 2023. Twenty-five statements reached consensus after two voting rounds by 24 Delphi panel experts. Inebilizumab and satralizumab have been listed in China, and off-label immunosuppressants and biologics are also used in clinical practice. However, there are no standard treatment recommendations in use of these biologics and maintenance therapy of NMOSD. Therefore, the interpretation of this consensus, focusing on the initial use of monoclonal drugs, the conversion between monoclonal drugs and immunosuppressants, as well as the application and safety of special populations, is conducive to improving the normative and effective use of of monoclonal drugs in NMOSD y ophthalmologists and neurologists

Citation： Li Yuyu, Wei Shihui, Zhou Huanfen. Interpret of international Delphi consensus on the management of aquaporin-4 immunoglobulin G seropositive neuromyelitis optica spectrum disorder. Chinese Journal of Ocular Fundus Diseases, 2023, 39(7): 525-529. doi: 10.3760/cma.j.cn511434-20230621-00281 Copy

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6.	Prain K, Woodhall M, Vincent A, et alAQP4 antibody assay sensitivity comparison in the era of the 2015 diagnostic criteria for NMOSD[J]. Front Neurol2019101028. DOI: 10.3389/fneur.2019.01028.
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13.	Chen T, Lennon VA, Liu YU, et alAstrocyte-microglia interaction drives evolving neuromyelitis optica lesion[J]. J Clin Invest2020130840254038. doi:10.1172/JCI134816.
14.	Ringelstein M, Ayzenberg I, Lindenblatt G, et alInterleukin-6 receptor blockade in treatment-refractory MOG-IgG-associated disease and neuromyelitis optica spectrum disorders[J]. Neurol Neuroimmunol Neuroinflamm202291e1100. DOI: 10.1212/NXI.0000000000001100.
15.	Pittock SJ, Lennon VA, McKeon A, et alEculizumab in AQP4-IgG-positive relapsing neuromyelitis optica spectrum disorders: an open-label pilot study[J]. Lancet Neurol2013126554562. DOI: 10.1016/S1474-4422(13)70076-0.
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19.	Diamond IR, Grant RC, Feldman BM, et alDefining consensus: a systematic review recommends methodologic criteria for reporting of Delphi studies[J]. J Clin Epidemiol2014674401409. DOI: 10.1016/j.jclinepi.2013.12.002.
20.	Pittock SJ, Berthele A, Fujihara K, et alEculizumab in Aquaporin-4-positive neuromyelitis optica spectrum disorder[J]. N Engl J Med20193817614625. DOI: 10.1056/NEJMoa1900866.
21.	Traboulsee A, Greenberg BM, Bennett JL, et al. Safety and efficacy of satralizumab monotherapy in neuromyelitis optica spectrum disorder: a randomised, double-blind, multicentre, placebo-controlled phase 3 trial[J]. Lancet Neurol, 2020, 19(5): 402-412. DOI: 10.1016/S1474-4422(20)30078-8.
22.	Beekman J, Keisler A, Pedraza O, et alNeuromyelitis optica spectrum disorder: patient experience and quality of life[J]. Neurol Neuroimmunol Neuroinflamm201964e580. DOI: 10.1212/NXI.0000000000000580.
23.	Brod SA. Review of approved NMO therapies based on mechanism of action, efficacy and long-term effects[J/OL]. Mult Scler Relat Disord, 2020, 46: 102538[2020-10-07]. https://linkinghub.elsevier.com/retrieve/pii/S2211-0348(20)30612-X. DOI: 10.1016/j.msard.2020.102538.
24.	Kim SH, Hyun JW, Joung A, et alPredictors of response to first-line immunosuppressive therapy in neuromyelitis optica spectrum disorders[J]. Mult Scler2017231419021908. DOI: 10.1177/1352458516687403.
25.	Youssef J, Novosad SA, Winthrop KLInfection risk and safety of corticosteroid use[J]. Rheum Dis Clin North Am2016421157176. DOI: 10.1016/j.rdc.2015.08.004.
26.	Tamez-Pérez HE, Quintanilla-Flores DL, Rodríguez-Gutiérrez R, et alSteroid hyperglycemia: prevalence, early detection and therapeutic recommendations: a narrative review[J]. World J Diabetes20156810731081. DOI: 10.4239/wjd.v6.i8.1073.
27.	Phulke S, Kaushik S, Kaur S, et alSteroid-induced glaucoma: an avoidable irreversible blindness[J]. J Curr Glaucoma Pract20171126772. DOI: 10.5005/jp-journals-l0028-1226.
28.	Lambrinoudaki I, Kung AWManagement of steroid-induced osteoporosis[J]. Chin Med J (Engl)20001138681685.
29.	Borisow N, Hellwig K, Paul FNeuromyelitis optica spectrum disorders and pregnancy: relapse-preventive measures and personalized treatment strategies[J]. EPMA J201893249256. DOI: 10.1007/s13167-018-0143-9.
30.	D’Souza R, Wuebbolt D, Andrejevic K, et al. Pregnancy and neuromyelitis optica spectrum disorder-reciprocal effects and practical recommendations: a systematic review[J/OL]. Front Neurol, 2020, 11: 544434[2020-10-16]. https://europepmc.org/article/MED/33178102. DOI: 10.3389/fneur.2020.544434.
31.	Mao-Draayer Y, Thiel S, Mills EA, et alNeuromyelitis optica spectrum disorders and pregnancy: therapeutic considerations[J]. Nat Rev Neurol2020163154170. DOI: 10.1038/s41582-020-0313-y.
32.	Mori S, Ueki Y, Hirakata N, et alImpact of tocilizumab therapy on antibody response to influenza vaccine in patients with rheumatoid arthritis[J]. Ann Rheum Dis2012711220062010. DOI: 10.1136/annrheumdis-2012-201950.
33.	Cheng DR, Barton R, Greenway A, et alRituximab and protection from vaccine preventable diseases: applying the evidence to pediatric patients[J]. Expert Rev Vaccines2016151215671574. DOI: 10.1080/14760584.2016.1193438.
34.	Andrade P, Santos-Antunes J, Rodrigues S, et alTreatment with infliximab or azathioprine negatively impact the efficacy of hepatitis B vaccine in inflammatory bowel disease patients[J]. J Gastroenterol Hepatol2015301115911595. DOI: 10.1111/jgh.13001.
35.	Smith KG, Isbel NM, Catton MG, et alSuppression of the humoral immune response by mycophenolate mofetil[J]. Nephrol Dial Transplant1998131160164. DOI: 10.1093/ndt/13.1.160.
36.	Aktas O, Smith MA, Rees WA, et alSerum glial fibrillary acidic protein: a neuromyelitis optica spectrum disorder biomarker[J]. Ann Neurol2021895895910. DOI: 10.1002/ana.26067.
37.	Chang X, Huang W, Wang L, et al. Serum neurofilament light and GFAP are associated with disease severity in inflammatory disorders with aquaporin-4 or myelin oligodendrocyte glycoprotein antibodies[J/OL]. Front Immunol, 2021, 12: 647618[2021-03-16]. https://europepmc.org/article/MED/33796113. DOI: 10.3389/fimmu.2021.647618.
38.	Kim HJ, Nakashima I, Viswanathan S, et al. 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[J/OL]. Mult Scler Relat Disord, 2021, 50: 102849[2021-02-20]. https://linkinghub.elsevier.com/retrieve/pii/S2211-0348(21)00115-2. DOI: 10.1016/j.msard.2021.102849.
39.	Pittock SJ, Fujihara K, Palace J, et alEculizumab monotherapy for NMOSD: data from PREVENT and its open-label extension[J]. Mult Scler2022283480486. DOI: 10.1177/13524585211038291.
40.	Nishimura J, Yamamoto M, Hayashi S, et alGenetic variants in C5 and poor response to eculizumab[J]. N Engl J Med20143707632639. DOI: 10.1056/NEJMoa1311084.
41.	Kim HJ, Paul F, Lana-Peixoto MA, et alMRI characteristics of neuromyelitis optica spectrum disorder: an international update[J]. Neurology2015841111651173. DOI: 10.1212/WNL.0000000000001367.

1. Jarius S, Paul F, Weinshenker BG, et alNeuromyelitis optica[J]. Nat Rev Dis Primers20206185. DOI: 10.1038/s41572-020-0214-9.
2. Wingerchuk DM, Banwell B, Bennett JL, et alInternational consensus diagnostic criteria for neuromyelitis optica spectrum disorders[J]. Neurology2015852177189. DOI: 10.1212/WNL.0000000000001729.
3. Papp V, Magyari M, Aktas O, et alWorldwide incidence and prevalence of neuromyelitis optica: a systematic review[J]. Neurology20219625977. DOI: 10.1212/WNL.0000000000011153.
4. Hor JY, Asgari N, Nakashima I, et alEpidemiology of neuromyelitis optica spectrum disorder and its prevalence and incidence worldwide[J]. Front Neurol202011501. DOI: 10.3389/fneur.2020.00501.
5. Hyun JW, Jeong IH, Joung A, et alEvaluation of the 2015 diagnostic criteria for neuromyelitis optica spectrum disorder[J]. Neurology2016861917721779. DOI: 10.1212/WNL.0000000000002655.
6. Prain K, Woodhall M, Vincent A, et alAQP4 antibody assay sensitivity comparison in the era of the 2015 diagnostic criteria for NMOSD[J]. Front Neurol2019101028. DOI: 10.3389/fneur.2019.01028.
7. Lennon VA, Wingerchuk DM, Kryzer TJ, et alA serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis[J]. Lancet2004364945121062012. DOI: 10.1016/S0140-6736(04)17551-X.
8. Kimbrough DJ, Fujihara K, Jacob A, et alTreatment of neuromyelitis optica: review and recommendations[J]. Mult Scler Relat Disord201214180187. DOI: 10.1016/j.msard.2012.06.002.
9. Trebst C, Jarius S, Berthele A, et alUpdate on the diagnosis and treatment of neuromyelitis optica: recommendations of the Neuromyelitis Optica Study Group (NEMOS) [J]. J Neurol20142611116. DOI: 10.1007/s00415-013-7169-7.
10. 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)[J]. 中国神经免疫学和神经病学杂志2021286423436. DOI:10.3969/j.issn.1006-2963.2021.06.002..Chinese Society of Immunology Neuroimmunology BranchGuidelines for diagnosis and treatment of neuromyelitis spectrum diseases in China (2021)[J]. Chin J Neuroimmunol & Neurol2021286423436. DOI:10.3969/j.issn.1006-2963.2021.06.002.
11. 中华医学会眼科学分会神经眼科学组中国脱髓鞘性视神经炎诊断和治疗循证指南(2021年)[J]. 中华眼科杂志2021573171186. DOI: 10.3760/cma.j.cn112142-20201124-00769..Neuro-ophthalmology Group of Ophthalmology Branch of Chinese Medical AssociationEvidence-based guidelines for diagnosis and treatment of demyelinating optic neuritis in China (2021)[J]. Chin J Ophthalmol2021573171186. DOI: 10.3760/cma.j.cn112142-20201124-00769.
12. Sellner J, Boggild M, Clanet M, et alEFNS guidelines on diagnosis and management of neuromyelitis optica[J]. Eur J Neurol201017810191032. DOI: 10.1111/j.1468-1331.2010.03066.x.
13. Chen T, Lennon VA, Liu YU, et alAstrocyte-microglia interaction drives evolving neuromyelitis optica lesion[J]. J Clin Invest2020130840254038. doi:10.1172/JCI134816.
14. Ringelstein M, Ayzenberg I, Lindenblatt G, et alInterleukin-6 receptor blockade in treatment-refractory MOG-IgG-associated disease and neuromyelitis optica spectrum disorders[J]. Neurol Neuroimmunol Neuroinflamm202291e1100. DOI: 10.1212/NXI.0000000000001100.
15. Pittock SJ, Lennon VA, McKeon A, et alEculizumab in AQP4-IgG-positive relapsing neuromyelitis optica spectrum disorders: an open-label pilot study[J]. Lancet Neurol2013126554562. DOI: 10.1016/S1474-4422(13)70076-0.
16. Cree BAC, Bennett JL, Kim HJ, et alInebilizumab for the treatment of neuromyelitis optica spectrum disorder (N-MOmentum): a double-blind, randomised placebo-controlled phase 2/3 trial[J]. Lancet20193941020613521363. DOI: 10.1016/S0140-6736(19)31817-3.
17. Yamamura T, Kleiter I, Fujihara K, et alTrial of satralizumab in neuromyelitis optica spectrum disorder[J]. N Engl J Med20193812221142124. DOI: 10.1056/NEJMoa1901747.
18. Paul F, Marignier R, Palace J, et al. International Delphi consensus on the management of AQP4-IgG+NMOSD: recommendations for eculizumab, inebilizumab, and satralizumab[J/OL]. Neurol Neuroimmunol Neuroinflamm, 2023, 10: e200124[2023-05-31]. https://europepmc.org/article/MED/37258412. DOI: 10.1212/NXI.0000000000200124.
19. Diamond IR, Grant RC, Feldman BM, et alDefining consensus: a systematic review recommends methodologic criteria for reporting of Delphi studies[J]. J Clin Epidemiol2014674401409. DOI: 10.1016/j.jclinepi.2013.12.002.
20. Pittock SJ, Berthele A, Fujihara K, et alEculizumab in Aquaporin-4-positive neuromyelitis optica spectrum disorder[J]. N Engl J Med20193817614625. DOI: 10.1056/NEJMoa1900866.
21. Traboulsee A, Greenberg BM, Bennett JL, et al. Safety and efficacy of satralizumab monotherapy in neuromyelitis optica spectrum disorder: a randomised, double-blind, multicentre, placebo-controlled phase 3 trial[J]. Lancet Neurol, 2020, 19(5): 402-412. DOI: 10.1016/S1474-4422(20)30078-8.
22. Beekman J, Keisler A, Pedraza O, et alNeuromyelitis optica spectrum disorder: patient experience and quality of life[J]. Neurol Neuroimmunol Neuroinflamm201964e580. DOI: 10.1212/NXI.0000000000000580.
23. Brod SA. Review of approved NMO therapies based on mechanism of action, efficacy and long-term effects[J/OL]. Mult Scler Relat Disord, 2020, 46: 102538[2020-10-07]. https://linkinghub.elsevier.com/retrieve/pii/S2211-0348(20)30612-X. DOI: 10.1016/j.msard.2020.102538.
24. Kim SH, Hyun JW, Joung A, et alPredictors of response to first-line immunosuppressive therapy in neuromyelitis optica spectrum disorders[J]. Mult Scler2017231419021908. DOI: 10.1177/1352458516687403.
25. Youssef J, Novosad SA, Winthrop KLInfection risk and safety of corticosteroid use[J]. Rheum Dis Clin North Am2016421157176. DOI: 10.1016/j.rdc.2015.08.004.
26. Tamez-Pérez HE, Quintanilla-Flores DL, Rodríguez-Gutiérrez R, et alSteroid hyperglycemia: prevalence, early detection and therapeutic recommendations: a narrative review[J]. World J Diabetes20156810731081. DOI: 10.4239/wjd.v6.i8.1073.
27. Phulke S, Kaushik S, Kaur S, et alSteroid-induced glaucoma: an avoidable irreversible blindness[J]. J Curr Glaucoma Pract20171126772. DOI: 10.5005/jp-journals-l0028-1226.
28. Lambrinoudaki I, Kung AWManagement of steroid-induced osteoporosis[J]. Chin Med J (Engl)20001138681685.
29. Borisow N, Hellwig K, Paul FNeuromyelitis optica spectrum disorders and pregnancy: relapse-preventive measures and personalized treatment strategies[J]. EPMA J201893249256. DOI: 10.1007/s13167-018-0143-9.
30. D’Souza R, Wuebbolt D, Andrejevic K, et al. Pregnancy and neuromyelitis optica spectrum disorder-reciprocal effects and practical recommendations: a systematic review[J/OL]. Front Neurol, 2020, 11: 544434[2020-10-16]. https://europepmc.org/article/MED/33178102. DOI: 10.3389/fneur.2020.544434.
31. Mao-Draayer Y, Thiel S, Mills EA, et alNeuromyelitis optica spectrum disorders and pregnancy: therapeutic considerations[J]. Nat Rev Neurol2020163154170. DOI: 10.1038/s41582-020-0313-y.
32. Mori S, Ueki Y, Hirakata N, et alImpact of tocilizumab therapy on antibody response to influenza vaccine in patients with rheumatoid arthritis[J]. Ann Rheum Dis2012711220062010. DOI: 10.1136/annrheumdis-2012-201950.
33. Cheng DR, Barton R, Greenway A, et alRituximab and protection from vaccine preventable diseases: applying the evidence to pediatric patients[J]. Expert Rev Vaccines2016151215671574. DOI: 10.1080/14760584.2016.1193438.
34. Andrade P, Santos-Antunes J, Rodrigues S, et alTreatment with infliximab or azathioprine negatively impact the efficacy of hepatitis B vaccine in inflammatory bowel disease patients[J]. J Gastroenterol Hepatol2015301115911595. DOI: 10.1111/jgh.13001.
35. Smith KG, Isbel NM, Catton MG, et alSuppression of the humoral immune response by mycophenolate mofetil[J]. Nephrol Dial Transplant1998131160164. DOI: 10.1093/ndt/13.1.160.
36. Aktas O, Smith MA, Rees WA, et alSerum glial fibrillary acidic protein: a neuromyelitis optica spectrum disorder biomarker[J]. Ann Neurol2021895895910. DOI: 10.1002/ana.26067.
37. Chang X, Huang W, Wang L, et al. Serum neurofilament light and GFAP are associated with disease severity in inflammatory disorders with aquaporin-4 or myelin oligodendrocyte glycoprotein antibodies[J/OL]. Front Immunol, 2021, 12: 647618[2021-03-16]. https://europepmc.org/article/MED/33796113. DOI: 10.3389/fimmu.2021.647618.
38. Kim HJ, Nakashima I, Viswanathan S, et al. 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[J/OL]. Mult Scler Relat Disord, 2021, 50: 102849[2021-02-20]. https://linkinghub.elsevier.com/retrieve/pii/S2211-0348(21)00115-2. DOI: 10.1016/j.msard.2021.102849.
39. Pittock SJ, Fujihara K, Palace J, et alEculizumab monotherapy for NMOSD: data from PREVENT and its open-label extension[J]. Mult Scler2022283480486. DOI: 10.1177/13524585211038291.
40. Nishimura J, Yamamoto M, Hayashi S, et alGenetic variants in C5 and poor response to eculizumab[J]. N Engl J Med20143707632639. DOI: 10.1056/NEJMoa1311084.
41. Kim HJ, Paul F, Lana-Peixoto MA, et alMRI characteristics of neuromyelitis optica spectrum disorder: an international update[J]. Neurology2015841111651173. DOI: 10.1212/WNL.0000000000001367.

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Interpret of international Delphi consensus on the management of aquaporin-4 immunoglobulin G seropositive neuromyelitis optica spectrum disorder

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