Grey matter atrophy and its relationship with white matter lesions in patients with myelin oligodendrocyte glycoprotein antibody-associated disease, aquaporin-4 antibody-positive neuromyelitis optica spectrum disorder, and multiple sclerosis

Cortese, R.; Battaglini, M.; Prados, F.; Gentile, G.; Luchetti, L.; Bianchi, A.; Haider, L.; Jacob, A.; Palace, J.; Messina, S.; Paul, F.; Marignier, R.; Durand-Dubief, F.; de Medeiros Rimkus, C.; Apostolos Pereira, S.L.; Sato, D.K.; Filippi, M.; Rocca, M.A.; Cacciaguerra, L.; Rovira, À.; Sastre-Garriga, J.; Arrambide, G.; Liu, Y.; Duan, Y.; Gasperini, C.; Tortorella, C.; Ruggieri, S.; Amato, M.P.; Ulivelli, M.; Groppa, S.; Grothe, M.; Llufriu, S.; Sepulveda, M.; Lukas, C.; Bellenberg, B.; Schneider, R.; Sowa, P.; Celius, E.G.; Pröbstel, A.K.; Granziera, C.; Yaldizli, Ö.; Müller, J.; Stankoff, B.; Bodini, B.; Barkhof, F.; Ciccarelli, O.; De Stefano, N.

Grey matter atrophy and its relationship with white matter lesions in patients with myelin oligodendrocyte glycoprotein antibody-associated disease, aquaporin-4 antibody-positive neuromyelitis optica spectrum disorder, and multiple sclerosis

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Item Type:	Article
Title:	Grey matter atrophy and its relationship with white matter lesions in patients with myelin oligodendrocyte glycoprotein antibody-associated disease, aquaporin-4 antibody-positive neuromyelitis optica spectrum disorder, and multiple sclerosis
Creators:	Cortese, R. ORCID: https://orcid.org/0000-0002-9803-7914, Battaglini, M., Prados, F., Gentile, G., Luchetti, L., Bianchi, A. ORCID: https://orcid.org/0000-0001-5541-5818, Haider, L. ORCID: https://orcid.org/0000-0002-1556-1770, Jacob, A., Palace, J., Messina, S. ORCID: https://orcid.org/0000-0002-1134-5771, Paul, F. ORCID: https://orcid.org/0000-0002-6378-0070, Marignier, R. ORCID: https://orcid.org/0000-0002-5967-2800, Durand-Dubief, F., de Medeiros Rimkus, C., Apostolos Pereira, S.L., Sato, D.K., Filippi, M. ORCID: https://orcid.org/0000-0002-5485-0479, Rocca, M.A. ORCID: https://orcid.org/0000-0003-2358-4320, Cacciaguerra, L., Rovira, À. ORCID: https://orcid.org/0000-0002-2132-6750, Sastre-Garriga, J. ORCID: https://orcid.org/0000-0002-1589-2254, Arrambide, G., Liu, Y. ORCID: https://orcid.org/0000-0003-4352-5774, Duan, Y., Gasperini, C. ORCID: https://orcid.org/0000-0002-3959-4067, Tortorella, C., Ruggieri, S., Amato, M.P., Ulivelli, M., Groppa, S., Grothe, M. ORCID: https://orcid.org/0000-0002-7998-5310, Llufriu, S. ORCID: https://orcid.org/0000-0003-4273-9121, Sepulveda, M., Lukas, C. ORCID: https://orcid.org/0000-0002-8562-9697, Bellenberg, B., Schneider, R., Sowa, P., Celius, E.G., Pröbstel, A.K. ORCID: https://orcid.org/0000-0002-7748-1872, Granziera, C., Yaldizli, Ö., Müller, J. ORCID: https://orcid.org/0000-0003-1394-8231, Stankoff, B. ORCID: https://orcid.org/0000-0002-9631-4674, Bodini, B., Barkhof, F., Ciccarelli, O. and De Stefano, N.
Abstract:	OBJECTIVE: To evaluate: (1) the distribution of gray matter (GM) atrophy in myelin oligodendrocyte glycoprotein antibody-associated disease (MOGAD), aquaporin-4 antibody-positive neuromyelitis optica spectrum disorder (AQP4+NMOSD), and relapsing-remitting multiple sclerosis (RRMS); and (2) the relationship between GM volumes and white matter lesions in various brain regions within each disease. METHODS: A retrospective, multicenter analysis of magnetic resonance imaging data included patients with MOGAD/AQP4+NMOSD/RRMS in non-acute disease stage. Voxel-wise analyses and general linear models were used to evaluate the relevance of regional GM atrophy. For significant results (p < 0.05), volumes of atrophic areas are reported. RESULTS: We studied 135 MOGAD patients, 135 AQP4+NMOSD, 175 RRMS, and 144 healthy controls (HC). Compared with HC, MOGAD showed lower GM volumes in the temporal lobes, deep GM, insula, and cingulate cortex (75.79 cm(3)); AQP4+NMOSD in the occipital cortex (32.83 cm(3)); and RRMS diffusely in the GM (260.61 cm(3)). MOGAD showed more pronounced temporal cortex atrophy than RRMS (6.71 cm(3)), whereas AQP4+NMOSD displayed greater occipital cortex atrophy than RRMS (19.82 cm(3)). RRMS demonstrated more pronounced deep GM atrophy in comparison with MOGAD (27.90 cm(3)) and AQP4+NMOSD (47.04 cm(3)). In MOGAD, higher periventricular and cortical/juxtacortical lesions were linked to reduced temporal cortex, deep GM, and insula volumes. In RRMS, the diffuse GM atrophy was associated with lesions in all locations. AQP4+NMOSD showed no lesion/GM volume correlation. INTERPRETATION: GM atrophy is more widespread in RRMS compared with the other two conditions. MOGAD primarily affects the temporal cortex, whereas AQP4+NMOSD mainly involves the occipital cortex. In MOGAD and RRMS, lesion-related tract degeneration is associated with atrophy, but this link is absent in AQP4+NMOSD.
Keywords:	Aquaporin 4, Atrophy, Autoantibodies, Gray Matter, Magnetic Resonance Imaging, Relapsing-Remitting Multiple Sclerosis, Myelin-Oligodendrocyte Glycoprotein, Neuromyelitis Optica, Retrospective Studies, White Matter
Source:	Annals of Neurology
ISSN:	0364-5134
Publisher:	Wiley
Volume:	92
Number:	2
Page Range:	276-288
Date:	23 May 2024
Official Publication:	https://doi.org/10.1002/ana.26951
PubMed:	View item in PubMed

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