Assessment of disability and disease burden in neuromyelitis optica spectrum disorders in the CIRCLES Cohort.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
30 10 2024
30 10 2024
Historique:
received:
01
04
2024
accepted:
01
10
2024
medline:
31
10
2024
pubmed:
31
10
2024
entrez:
31
10
2024
Statut:
epublish
Résumé
Neuromyelitis optica spectrum disorders (NMOSD) comprise autoimmune diseases imposing substantial disability. We compared an NMOSD-targeted disability assessment of mobility, vision, and self-care domains (individually and composite) with the multiple sclerosis-targeted Expanded Disability Status Scale (EDSS) to assess NMOSD disease burden. An overall cohort (n = 505) and a subset of these patients with an enriched dataset (n = 198) were analyzed from the CIRCLES longitudinal, observational database of patients with AQP4-IgG-seropositive or -seronegative NMOSD in North America. Multinomial modeling was used to identify temporal correlates of disability improvement, stability, and worsening. Prior on-study relapse correlated with worsening mobility (OR, 3.08; 95% CI: 1.61-5.90), vision (OR, 3.99; 95% CI: 2.03-7.86), self-care disability (OR, 1.90; 95% CI: 1.07-3.38), and mean composite index disability (OR, 4.20; 95% CI: 1.71-10.34). Higher vision disability was associated with Black race, shorter time on-study, and AQP4-IgG-seropositive status in patients ≥ 18 years (p < 0.05). Disease onset phenotype and sex correlated with pain interference (p < 0.05). These correlates of NMOSD disability were undetected by EDSS. The CIRCLES real-world experience supports the need for NMOSD-specific disability assessment to improve recognition of disease burden, facilitate proactive clinical management, offer insights into resilience, and inform clinical trial design.
Identifiants
pubmed: 39477975
doi: 10.1038/s41598-024-75013-z
pii: 10.1038/s41598-024-75013-z
doi:
Substances chimiques
Aquaporin 4
0
Immunoglobulin G
0
Types de publication
Journal Article
Observational Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
26150Informations de copyright
© 2024. The Author(s).
Références
Kim, S. M. et al. Differential diagnosis of neuromyelitis optica spectrum disorders. Ther. Adv. Neurol. Disord. 10, 265–289. https://doi.org/10.1177/1756285617709723 (2017).
doi: 10.1177/1756285617709723
pubmed: 28670343
Huda, S. et al. Neuromyelitis optica spectrum disorders. Clin. Med. (Lond). 19, 169–176. https://doi.org/10.7861/clinmedicine.19-2-169 (2019).
doi: 10.7861/clinmedicine.19-2-169
pubmed: 30872305
Wingerchuk, D. M. et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology. 85, 177–189. https://doi.org/10.1212/WNL.0000000000001729 (2015).
doi: 10.1212/WNL.0000000000001729
pubmed: 26092914
Hor, J. Y. et al. Epidemiology of neuromyelitis optica spectrum disorder and its prevalence and incidence worldwide. Front. Neurol. 11, 501. https://doi.org/10.3389/fneur.2020.00501 (2020).
doi: 10.3389/fneur.2020.00501
pubmed: 32670177
Flanagan, E. P. et al. Epidemiology of aquaporin-4 autoimmunity and neuromyelitis optica spectrum. Ann. Neurol. 79, 775–783. https://doi.org/10.1002/ana.24617 (2016).
doi: 10.1002/ana.24617
pubmed: 26891082
Kurtzke, J. F. & Berlin, L. The effects of isoniazid on patients with multiple sclerosis; preliminary report. Am. Rev. Tuberc. 70, 577–592. https://doi.org/10.1164/art.1954.70.4.577 (1954).
doi: 10.1164/art.1954.70.4.577
pubmed: 13197736
Kurtzke, J. F. Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS). Neurology. 33, 1444–1452. https://doi.org/10.1212/wnl.33.11.1444 (1983).
doi: 10.1212/wnl.33.11.1444
pubmed: 6685237
Akaishi, T. et al. Progressive patterns of neurological disability in multiple sclerosis and neuromyelitis optica spectrum disorders. Sci. Rep. 10, 13890. https://doi.org/10.1038/s41598-020-70919-w (2020).
doi: 10.1038/s41598-020-70919-w
pubmed: 32807848
Wingerchuk, D. M., Noseworthy, J. H. & Weinshenker, B. G. Clinical outcome measures and rating scales in multiple sclerosis trials. Mayo Clin. Proc. 72, 1070–1079. https://doi.org/10.4065/72.11.1070 (1997)
Drulovic, J. et al. Long-term outcome and prognosis in patients with neuromyelitis optica spectrum disorder from Serbia. Mult Scler. Relat. Disord. 36, 101413. https://doi.org/10.1016/j.msard.2019.101413 (2019).
doi: 10.1016/j.msard.2019.101413
pubmed: 31586803
Quinn, T. J., Dawson, J., Walters, M. R. & Lees, K. R. Reliability of the modified Rankin Scale: a systematic review. Stroke. 40, 3393–3395. https://doi.org/10.1161/STROKEAHA.109.557256 (2009).
doi: 10.1161/STROKEAHA.109.557256
pubmed: 19679846
Rankin, J. Cerebral vascular accidents in patients over the age of 60. II. Prognosis. Scott. Med. J. 2, 200–215. https://doi.org/10.1177/003693305700200504 (1957).
doi: 10.1177/003693305700200504
pubmed: 13432835
Cook, L. J. et al. Collaborative International Research in Clinical and Longitudinal Experience Study in NMOSD. Neurol. Neuroimmunol. Neuroinflamm. 6, e583. https://doi.org/10.1212/NXI.0000000000000583 (2019).
doi: 10.1212/NXI.0000000000000583
pubmed: 31355319
Gholizadeh, S. et al. Clinical and epidemiological correlates of treatment change in patients with NMOSD: insights from the CIRCLES cohort. J. Neurol. 270, 2048–2058. https://doi.org/10.1007/s00415-022-11529-6 (2023).
doi: 10.1007/s00415-022-11529-6
pubmed: 36565348
West, S. K. et al. How does visual impairment affect performance on tasks of everyday life? The SEE Project. Salisbury Eye Evaluation. Arch. Ophthalmol. 120, 774–780. https://doi.org/10.1001/archopht.120.6.774 (2002).
doi: 10.1001/archopht.120.6.774
pubmed: 12049583
Zebardast, N. et al. Comparing the impact of refractive and nonrefractive vision loss on functioning and disability: the Salisbury Eye evaluation. Ophthalmology. 122, 1102–1110. https://doi.org/10.1016/j.ophtha.2015.02.024 (2015).
doi: 10.1016/j.ophtha.2015.02.024
pubmed: 25813453
Meyer-Moock, S., Feng, Y. S., Maeurer, M., Dippel, F. W. & Kohlmann, T. Systematic literature review and validity evaluation of the Expanded Disability Status Scale (EDSS) and the Multiple Sclerosis Functional Composite (MSFC) in patients with multiple sclerosis. BMC Neurol. 14, 58. https://doi.org/10.1186/1471-2377-14-58 (2014).
doi: 10.1186/1471-2377-14-58
pubmed: 24666846
Varma, R. et al. Visual impairment and blindness in adults in the United States: demographic and geographic variations from 2015 to 2050. JAMA Ophthalmol. 134, 802–809. https://doi.org/10.1001/jamaophthalmol.2016.1284 (2016).
doi: 10.1001/jamaophthalmol.2016.1284
pubmed: 27197072
Robbins, N. M. et al. Black patients matter in neurology: race, racism, and race-based neurodisparities. Neurology. 99, 106–114. https://doi.org/10.1212/wnl.0000000000200830 (2022).
doi: 10.1212/wnl.0000000000200830
pubmed: 35851551
Meca-Lallana, J. E. et al. Impact of neuromyelitis optica spectrum disorder on quality of life from the patients’ perspective: an observational cross-sectional study. Neurol. Ther. 11, 1101–1116. https://doi.org/10.1007/s40120-022-00356-6 (2022).
doi: 10.1007/s40120-022-00356-6
pubmed: 35524037
Hümmert, M. W. et al. Cognition in patients with neuromyelitis optica spectrum disorders: a prospective multicentre study of 217 patients (CogniNMO-Study). Mult Scler. 29, 819–831. https://doi.org/10.1177/13524585231151212 (2023).
doi: 10.1177/13524585231151212
pubmed: 36786424
Kadish, R. et al. Clinical burden of relapses in aquaporin-4 immunoglobulin G-positive neuromyelitis optica spectrum disorder: a single center cohort analysis. J. Neuroimmunol. 362, 577761. https://doi.org/10.1016/j.jneuroim.2021.577761 (2022).
doi: 10.1016/j.jneuroim.2021.577761
pubmed: 34823121
Khalilidehkordi, E. et al. Relapse patterns in NMOSD: evidence for earlier occurrence of optic neuritis and possible seasonal variation. Front. Neurol. 11, 537. https://doi.org/10.3389/fneur.2020.00537 (2020).
doi: 10.3389/fneur.2020.00537
pubmed: 32612571
Xie, Q., Sun, M., Sun, J., Zheng, T. & Wang, M. New progress in the treatment of neuromyelitis optica spectrum disorder with monoclonal antibodies (review). Exp. Ther. Med. 21, 148. https://doi.org/10.3892/etm.2020.9579 (2021).
doi: 10.3892/etm.2020.9579
pubmed: 33456515
Aktas, O. et al. Serum glial fibrillary acidic protein: a neuromyelitis optica spectrum disorder biomarker. Ann. Neurol. 89, 895–910. https://doi.org/10.1002/ana.26067 (2021).
doi: 10.1002/ana.26067
pubmed: 33724534
Gholizadeh, S. et al. Novel assessment of disability vs cognition and pain in neuromyelitis optica spectrum disorders: a CIRCLES cohort study. Mult Scler. 27 (2 suppl), 134–740 (2021).
Exuzides, A. et al. Novel disability assessment of neuromyelitis optica spectrum disorders derived from the CIRCLES experience. Poster presented at ECTRIMS: the virtual experience; October 13–15, 2021. (2021). P030.
Hohol, M. J., Orav, E. J. & Weiner, H. L. Disease steps in multiple sclerosis: a simple approach to evaluate disease progression. Neurology. 45, 251–255. https://doi.org/10.1212/wnl.45.2.251 (1995).
doi: 10.1212/wnl.45.2.251
pubmed: 7854521
Wingerchuk, D. M., Hogancamp, W. F., O’Brien, P. C. & Weinshenker, B. G. The clinical course of neuromyelitis optica (Devic’s syndrome). Neurology. 53, 1107–1114. https://doi.org/10.1212/wnl.53.5.1107 (1999).
doi: 10.1212/wnl.53.5.1107
pubmed: 10496275
Pittock, S. J. et al. Eculizumab in AQP4-IgG-positive relapsing neuromyelitis optica spectrum disorders: an open-label pilot study. Lancet Neurol. 12, 554–562. https://doi.org/10.1016/S1474-4422(13)70076-0 (2013).
doi: 10.1016/S1474-4422(13)70076-0
pubmed: 23623397
Hauser, S. L. et al. Intensive immunosuppression in progressive multiple sclerosis. A randomized, three-arm study of high-dose intravenous cyclophosphamide, plasma exchange, and ACTH. N Engl. J. Med. 308, 173–180. https://doi.org/10.1056/NEJM198301273080401 (1983).
doi: 10.1056/NEJM198301273080401
pubmed: 6294517
Whitaker, J. N., McFarland, H. F., Rudge, P. & Reingold, S. C. Outcomes assessment in multiple sclerosis clinical trials: a critical analysis. Mult Scler. 1, 37–47. https://doi.org/10.1177/135245859500100107 (1995).
doi: 10.1177/135245859500100107
pubmed: 9345468
Rudick, R. et al. Clinical outcomes assessment in multiple sclerosis. Ann. Neurol. 40, 469–479. https://doi.org/10.1002/ana.410400321 (1996).
doi: 10.1002/ana.410400321
pubmed: 8797541
Cutter, G. R. et al. Development of a multiple sclerosis functional composite as a clinical trial outcome measure. Brain. 122 (Pt 5), 871–882. https://doi.org/10.1093/brain/122.5.871 (1999).
doi: 10.1093/brain/122.5.871
pubmed: 10355672
Cohen, J. A. et al. Use of the multiple sclerosis functional composite as an outcome measure in a phase 3 clinical trial. Arch. Neurol. 58, 961–967. https://doi.org/10.1001/archneur.58.6.961 (2001).
doi: 10.1001/archneur.58.6.961
pubmed: 11405811
Quinn, T. J., Dawson, J., Walters, M. R. & Lees, K. R. Variability in modified Rankin scoring across a large cohort of international observers. Stroke. 39, 2975–2979. https://doi.org/10.1161/STROKEAHA.108.515262 (2008).
doi: 10.1161/STROKEAHA.108.515262
pubmed: 18688002
Mahoney, F. I. & Barthel, D. W. Functional evaluation: the Barthel Index. Md. State Med. J. 14, 61–65 (1965).
pubmed: 14258950
Shah, S., Vanclay, F. & Cooper, B. Improving the sensitivity of the Barthel Index for stroke rehabilitation. J. Clin. Epidemiol. 42, 703–709. https://doi.org/10.1016/0895-4356(89)90065-6 (1989).
doi: 10.1016/0895-4356(89)90065-6
pubmed: 2760661
Lawton, M. P. & Brody, E. M. Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist. 9, 179–186 (1969).
doi: 10.1093/geront/9.3_Part_1.179
pubmed: 5349366
Dufournet, M. et al. Proposition of a corrected measure of the Lawton instrumental activities of daily living score. BMC Geriatr. 21, 39. https://doi.org/10.1186/s12877-020-01995-w (2021).
doi: 10.1186/s12877-020-01995-w
pubmed: 33430781
Mishel, M. H. The measurement of uncertainty in illness. Nurs. Res. 30, 258–263 (1981).
doi: 10.1097/00006199-198109000-00002
pubmed: 6912987