Safety and efficacy of tocilizumab versus azathioprine in highly relapsing neuromyelitis optica spectrum disorder (TANGO): an open-label, multicentre, randomised, phase 2 trial
Open accessAbstract
Background Azathioprine is used as a first-line treatment to prevent relapses of neuromyelitis optica spectrum disorder (NMOSD). Tocilizumab has been reported to reduce NMOSD disease activity in retrospective case reports. We aimed to compare the safety and efficacy of tocilizumab and azathioprine in patients with highly relapsing NMOSD. Methods We did an open-label, multicentre, randomised, phase 2 trial at six hospitals in China. We recruited adult patients (aged ≥18 years) with highly relapsing NMOSD diagnosed according to 2015 International Panel for Neuromyelitis Optica Diagnosis criteria, who had an Expanded Disability Status Scale (EDSS) score of 7·5 or lower, and had a history of at least two clinical relapses during the previous 12 months or three relapses during the previous 24 months with at least one relapse within the previous 12 months. Patients were randomly assigned (1:1) to intravenous tocilizumab (8 mg/kg every 4 weeks) or oral azathioprine (2-3 mg/kg per day) by an independent statistician using computer-generated randomisation software with permuted blocks of four. The central review committee, EDSS raters, laboratory personnel, and radiologists were masked to the treatment assignment, but investigators and patients were aware of treatment allocation. The minimum planned duration of treatment was 60 weeks following randomisation. The primary outcome was time to first relapse in the full analysis set, which included all randomly assigned patients who received at least one dose of study drug, and the per-protocol population, which included all patients who used azathioprine or tocilizumab as monotherapy. For the analyses of the primary outcome, the patients were prespecified into two subgroups according to concomitant autoimmune disease status. Safety was assessed in the full analysis set. This study is registered with ClinicalTrials.gov, NCT03350633. Findings Between Nov 1, 2017, and Aug 3, 2018, we enrolled 118 patients, of whom 59 were randomly assigned to tocilizumab and 59 were randomly assigned to azathioprine. All 118 patients received one dose of study drug and were included in the full analysis set. 108 participants were included in the per-protocol analysis (56 in the tocilizumab group and 52 in the azathioprine group). In the full analysis set, median time to the first relapse was longer in the tocilizumab group than the azathioprine group (78·9 weeks [IQR 58·3-90·6] vs 56·7 [32·9-81·7] weeks; p=0·0026). Eight (14%) of 59 patients in the tocilizumab group and 28 (47%) of 59 patients in the azathioprine group had a relapse at the end of the study (hazard ratio [HR] 0·236 [95% CI 0·107-0·518]; p<0·0001). In the per-protocol analysis, 50 (89%) of 56 patients in the tocilizumab group were relapse-free compared with 29 (56%) of 52 patients in the azathioprine group at the end of the study (HR 0·188 [95% CI 0·076-0·463]; p<0·0001); the median time to first relapse was also longer in the tocilizumab group than the azathioprine group (67·2 weeks [IQR 47·9-77·9] vs 38·0 [23·6-64·9]; p<0·0001). In the prespecified subgroup analysis of the full analysis set stratified by concomitant autoimmune diseases, among patients without concomitant autoimmune diseases, three (9%) of 34 patients in the tocilizumab group and 13 (35%) of 37 patients in the azathioprine group had relapsed by the end of the study. Among patients with concomitant autoimmune diseases, a lower proportion of patients in the tocilizumab group had a relapse than in the azathioprine group (five [20%] of 25 patients vs 15 [68%] of 22 patients; HR 0·192 [95% CI 0·070-0·531]; p=0·0004). 57 (97%) of 59 patients in the tocilizumab group and 56 (95%) of 59 patients in the azathioprine group had adverse events. Treatment-associated adverse events occurred in 36 (61%) of 59 tocilizumab-treated patients and 49 (83%) of 59 azathioprine-treated patients. One death (2%) occurred in the tocilizumab group and one (2%) in the azathioprine group, but neither of the deaths were treatment-related. Interpretation Tocilizumab significantly reduced the risk of a subsequent NMOSD relapse compared with azathioprine. Tocilizumab might therefore be another safe and effective treatment to prevent relapses in patients with NMOSD. Funding Tianjin Medical University, Advanced Innovation Center for Human Brain Protection, National Key Research and Development Program of China, National Science Foundation of China.
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The long-term persistence of (re-)activatable autoantigen-specific ThEx cells in patients in remission may well explain the less-than-perfect treatment efficacy of steroid-sparing agents, depletion of CD19/CD20 memory B cells, as well as exacerbation of disease by b-IFN.
“In any case, the long-term persistence of (re-)activatable autoantigen-specific ThEx cells in patients in remission may well explain the less-than-perfect treatment efficacy of steroid-sparing agents, 64-67 depletion of CD19/CD20 memory B cells, 68,69 as well as exacerbation of disease by b -IFN. 27,70”
From Autoantigen-specific CD4+ T cells acquire an exhausted phenotype and persist in human antigen-specific autoimmune diseases (2024) · cites this paper as [66]
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Advances in the Treatment of Neuromyelitis Optica Spectrum Disorder
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“An open-label randomized phase 2 trial (TANGO) included 118 patients with active NMOSD who were randomized 1:1 to either tocilizumab, 8 mg/kg, monthly IV infusions or azathioprine, 2 to 3 mg/kg, oral daily.(4) Analysis of the primary outcome of time to first relapse favored tocilizumab over azathioprine with a median…”
BackgroundMethodAdverse Events in NMOSD Therapy
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“, one as due to “central respiratory failure secondary to myelitis involving the high cervical spine and medulla oblongata”, the other to “severe myelitis” [41,44].”
BackgroundMethodNeuromyelitis Optica Spectrum Disorders
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“Tocilizumab has recently demonstrated its efficacy in patients with ICI-related cerebritis(5) and other non-ICI-related CNS inflammatory conditions, such as neuromyelitis optica spectrum disorder (NMOSD).(6) Similarly, ruxolitinib was also effective in a patient with severe NMOSD.”
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Neuromyelitis Optica Spectrum Disorder Treatment—Current and Future Prospects
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“An openlabel, multicenter, randomized phase 2 trial (TANGO) [65] demonstrated the advantage of tocilizumab over AZA in achieving clinical endpoints (reduced relapse rate and sustained disability), with a small percentage of severe outcomes and a mild increase in transaminases as the main adverse effects [29,64,66].”
BackgroundIn‐depth peripheral CD4+ T profile correlates with myasthenic crisis
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“26 Although the numbers for immunotherapies other than rituximab and eculizumab were relatively small in our study, we could support this observation and validate these findings for NMOSD in our multivariate model for rituximab and eculizumab.”
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Drug Treatment of Neuromyelitis Optica Spectrum Disorders: Out with the Old, in with the New?
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“antibody, was compared head-to-head to azathioprine in a randomized, open-label TANGO trial [182].”
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Treatment and Relapse Prevention of Typical and Atypical Optic Neuritis
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“The authors concluded that tocilizumab significantly reduced the risk of relapse compared with azathioprine in NMOSD, proposing the agent as a potentially effective and safe treatment for relapse prevention in NMOSD [107,132].”
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Responsiveness to Tocilizumab in Anti-Acetylcholine Receptor-Positive Generalized Myasthenia Gravis
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“Several randomized controlled trials have shown the effectiveness of tocilizumab in autoimmune diseases including rheumatoid diseases and neuromyelitis optica spectrum disorders [9, 10].”
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Efficacy and safety of tocilizumab in patients with refractory generalized myasthenia gravis
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Outcomes of coronavirus disease 2019 in patients with neuromyelitis optica and associated disorders
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“Interestingly, monoclonal antibodies such as anti-IL6 receptors (satralizumab, tocilizumab)[4,5] and C5 inhibitors (eculizumab)[6], known to reduce relapse rate in NMOSD, are currently being tested in clinical trials in COVID-19-related acute respiratory distress syndrome due to their possible effect on the ‘cytokine…”
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Optic neuritis: current challenges in diagnosis and management
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“Copyright © 2023 Wolters Kluwer H new IL-6 inhibitors specifically designed for NMOSD [45].”
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“Tocilizumab also decreases serum AQP4-IgG titers in patients with highly active NMOSD (15).”
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“This work was supported by the National Natural Science Foundation of China (Grant no. 82072079).”
BackgroundInfluentialEmerging drugs for the treatment of neuromyelitis optica
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“For example, RTX and inebilizumab [12–14] target antibody-producing B cells, eculizumab [15] targets complement protein C5, and tocilizumab [16] and satralizumab [17, 18] block interleukin-6 (IL-6) signaling.”
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Satralizumab in the Treatment of Neuromyelitis Optica Spectrum Disorder
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New Therapeutic Landscape in Neuromyelitis Optica
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Immuno-pathogenesis of neuromyelitis optica and emerging therapies
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Pediatric Neuromyelitis Optica Spectrum Disorder
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“37 However, it is noteworthy that each of these studies included only approximately 15–20 sero-negative NMOSD patients, and the Satralizumab trials relied on ELISA to detect AQP4-IgG, which has a sensitivity of 60%.”
Proinflammatory cytokines and their receptors as druggable targets to alleviate pathological pain
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Emerging Targeted Therapies for Neuromyelitis Optica Spectrum Disorders
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Treatment of myelin oligodendrocyte glycoprotein immunoglobulin G–associated disease
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Efficacy and safety of Tocilizumab for thyroid eye disease: a systemic review and Meta-analysis
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“Similarly, a previous RCT in rheumatoid arthritis showed no difference between intravenous TCZ (8 mg/kg every 4 weeks) and subcutaneous TCZ (162 mg/kg weekly) [42], supporting our subgroup findings.”
Emerging Role of Targeted Monoclonal Antibodies in Neuromyelitis Optica Spectrum Disorders
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“Due to the multiple sites of action of IL-6 and a favorable safety profile in early rheumatology cohorts, tocilizumab has been studied for many other indications over the past 15 years, including refractory Takayasu disease [31], systemic lupus erythematosus [32], giant cell arteritis [33], highly relapsing neuromyeli…”
BackgroundPathogenic antibodies to AQP4: Neuromyelitis optica spectrum disorder (NMOSD)
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“Furthermore, the TANGO study suggested that tocilizumab provides evident clinical efficacy for patients with NMOSD regardless of their autoimmune disease status [14].”
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Gholizadeh, S., Exuzides, A., Lewis, K. E., Palmer, C. A., Waltz, M., ROSE, J. W., Jolley, A. M., Behne, J. M., Behne, M. K., Blaschke, T. F., et al. (2022) · Journal of Neurology · doi:10.1007/s00415-022-11529-6 · Cited by 14 · see citing works
“In parallel, a recent open-label study of tocilizumab in a small number of patients with NMOSD (TANGO) [30] applied the IPND criteria and reported a 26% reduction in relapse risk compared with azathioprine.”
- Authors
- Zhang, C., Zhang, M., Qiu, W., Ma, H., Zhang, X., Zhu, Z., Yang, C.-S., Jia, D., Zhang, T.-X., Yuan, M., Feng, Y., Yang, L., Lu, W., Yu, C., Bennett, J. L., & Shi, F.-D.
- Affiliations
- Capital Medical University (CN)
- Shanxi Medical University (CN)
- Sun Yat-sen University (CN)
- Tianjin Huanhu Hospital (CN)
- Tianjin Medical University General Hospital (CN)
- Tianjin Medical University (CN)
- University of Colorado Anschutz (US)
- Corresponding author
- Shi, Fu-Dong
- ORCID
- Venue
- The Lancet Neurology
- Publisher
- Elsevier BV
- Published
- 2020-05
- Volume
- 19
- Issue
- 5
- Pages
- 391-401
- ISSN
- 1474-4422 (ISSN-L)
- PMC
- PMC7935423
- OpenAlex
- W3019956952
- Cited by
- 287
- References
- 27
- Citations by year
- 2026: 34 · 2025: 31 · 2024: 37 · 2023: 49 · 2022: 54 · 2021: 53 · 2020: 26
- FWCI
- 29.30
- Type
- journal article
- Language
- en
- Update notices
- erratum (2025-12-01)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- The Lancet Neurology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Guthy-Jackson Charitable Foundation
- AbbVie
- Roche
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Health Sciences › Medicine › Neurology › Peripheral Neuropathies and Disorders
- Health Sciences › Medicine › Ophthalmology › Drug-Induced Ocular Toxicity
- Keywords
- neuromyelitis optica spectrum disorder, tocilizumab, azathioprine, relapse prevention, time to first relapse, IL-6 inhibition, immunosuppressive therapy, concomitant autoimmune disease, treatment safety, Expanded Disability Status Scale, disease-modifying therapy, China
- MeSH terms
- Adult, Azathioprine, Female, Humans, Immunosuppressive Agents, Male, Middle Aged, Neuromyelitis Optica, Treatment Outcome, Antibodies, Monoclonal, Humanized
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