Restricted accessResearch articleFirst published online 2022-4
Cortical involvement and leptomeningeal inflammation in myelin oligodendrocyte glycoprotein antibody disease: A three-dimensional fluid-attenuated inversion recovery MRI study
Cortical demyelination and meningeal inflammation have been detected neuropathologically in multiple sclerosis (MS) and recently in myelin oligodendrocyte glycoprotein antibody disease (MOGAD).
Objectives:
To assess in vivo cortical and leptomeningeal involvement in MOGAD.
Methods:
We prospectively evaluated 11 MOGAD and 12 relapsing-remitting MS (RRMS) patients combining three-dimensional fluid-attenuated inversion recovery (3D-FLAIR) and 3D-T1-weighted (3D-T1w) sequences at 3-Tesla magnetic resonance imaging (MRI). Leptomeningeal contrast enhancement (LMCE) was assessed on 3D-FLAIR post-gadolinium (3D-FLAIRGd). Cerebral cortical lesions (CCLs) were classified as either intracortical–subpial (IC–SP) or leukocortical (LC).
Results:
CCLs were present in 8/11 MOGAD and 12/12 RRMS patients, with the number of CCLs being significantly lower in MOGAD (median (interquartile range (IQR)) 3 (0.5–4) vs 12 (4.75–19), p = 0.0032). In MOGAD, IC–SP lesions were slightly more prevalent than LC lesions (2 (0–2.5) vs 1 (0–2), p = 0.6579); whereas in RRMS, IC–SP lesions were less prevalent than LC lesions (3.5 (2.75–5.5) vs 9 (2–12.75), p = 0.27). LMCE was observed in 3/11 MOGAD and 1/12 RRMS patients; MOGAD with LMCE showed an increased median number of CCLs compared with MOGAD without LMCE (8 (4–9) vs 2.5 (0.75–3.25), p = 0.34). No correlation was observed between MOGAD MRI findings and (a) MOGAD duration, (b) serum MOG-immunoglobulin G1 titers, and (c) oligoclonal band presence.
Conclusion:
We described cortical lesion topography and detected for the first time LMCE using 3D-FLAIRGd sequences in MOGAD patients.
HowellOWReevesCANicholasR, et al. Meningeal inflammation is widespread and linked to cortical pathology in multiple sclerosis. Brain2011; 134(Pt 9): 2755–2771.
2.
SerafiniBRosicarelliBMagliozziR, et al. Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol2004; 14(2): 164–174.
3.
MagliozziRHowellOVoraA, et al. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain2007; 130(Pt 4): 1089–1104.
4.
LucchinettiCFPopescuBFGBunyanRF, et al. Inflammatory cortical demyelination in early multiple sclerosis. N Engl J Med2011; 365: 2188–2197.
5.
PetersonJWBöLMörkS, et al. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol2001; 50(3): 389–400.
6.
BøLVedelerCANylandHI, et al. Subpial demyelination in the cerebral cortex of multiple sclerosis patients. J Neuropathol Exp Neurol2003; 62(7): 723–732.
7.
FilippiMRoccaMA.Novel MRI approaches to assess patients with multiple sclerosis. Curr Opin Neurol2010; 23(3): 212–217.
8.
PolakPMagnanoCZivadinovR, et al. 3D FLAIRED: 3D fluid attenuated inversion recovery for enhanced detection of lesions in multiple sclerosis. Magn Reson Med2012; 68(3): 874–881.
9.
MikeAGlanzBIHildenbrandP, et al. Identification and clinical impact of multiple sclerosis cortical lesions as assessed by routine 3T MR imaging. Am J Neuroradiol2011; 32(3): 515–521.
10.
HarrisonDMRoySOhJ, et al. Association of cortical lesion burden on 7-T magnetic resonance imaging with cognition and disability in multiple sclerosis. JAMA Neurol2015; 72(9): 1004–1012.
11.
KilsdonkIDde GraafWLSorianoAL, et al. Multicontrast MR imaging at 7T in multiple sclerosis: Highest lesion detection in cortical gray matter with 3D-FLAIR. Am J Neuroradiol2013; 34(4): 791–796.
12.
AbsintaMVuoloLRaoA, et al. Gadolinium-based MRI characterization of leptomeningeal inflammation in multiple sclerosis. Neurology2015; 85: 18–28.
13.
ZivadinovRRamasamyDPVaneckovaM, et al. Leptomeningeal contrast enhancement is associated with progression of cortical atrophy in MS: A retrospective, pilot, observational longitudinal study. Mult Scler2017; 23(10): 1336–1345.
14.
BergslandNRamasamyDTavazziE, et al. Leptomeningeal contrast enhancement is related to focal cortical thinning in relapsing-remitting multiple sclerosis: A cross-sectional MRI study. Am J Neuroradiol2019; 40(4): 620–625.
15.
Cobo-CalvoARuizAMaillartE, et al. Clinical spectrum and prognostic value of CNS MOG autoimmunity in adults: The MOGADOR study. Neurology2018; 90: e1858–e1869.
16.
JariusSRuprechtKKleiterI, et al. MOG-IgG in NMO and related disorders: A multicenter study of 50 patients. Part 2: Epidemiology, clinical presentation, radiological and laboratory features, treatment responses, and long-term outcome. J Neuroinflammation2016; 13: 280.
17.
HöftbergerRGuoYFlanaganEP, et al. The pathology of central nervous system inflammatory demyelinating disease accompanying myelin oligodendrocyte glycoprotein autoantibody. Acta Neuropathol2020; 139(5): 875–892.
18.
TakaiYMisuTKanekoK, et al. Myelin oligodendrocyte glycoprotein antibody-associated disease: An immunopathological study. Brain2020; 143: 1431–1446.
19.
LiHYangLWuZ, et al. Brain MRI features of Chinese Han patients with MOG-anitbody disease. Mult Scler Relat Disord2020; 43: 102167.
20.
DuanYZhuoZLiH, et al. Brain structural alterations in MOG antibody diseases: A comparative study with AQP4 seropositive NMOSD and MS. J Neurol Neurosurg Psychiatry2021; 92(7): 709–716.
21.
SalamaSKhanMShanechiA, et al. MRI differences between MOG antibody disease and AQP4 NMOSD. Mult Scler2020; 26(14): 1854–1865.
22.
JurynczykMGeraldesRProbertF, et al. Distinct brain imaging characteristics of autoantibody-mediated CNS conditions and multiple sclerosis. Brain2017; 140: 617–627.
23.
TzartosJSKaragiorgouKTzanetakosD, et al. Deciphering anti-MOG IgG antibodies: Clinical and radiological spectrum, and comparison of antibody detection assays. J Neurol Sci2020; 410: 116673.
24.
ThompsonAJBanwellBLBarkhofF, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol2018; 17: 162–173.
25.
FilippiMPreziosaPBanwellBL, et al. Assessment of lesions on magnetic resonance imaging in multiple sclerosis: Practical guidelines. Brain2019; 142: 1858–1875.
NelsonFPoonawallaAHouP, et al. 3D MPRAGE improves classification of cortical lesions in multiple sclerosis. Mult Scler2008; 14(9): 1214–1219.
28.
FukuokaHHiraiTOkudaT, et al. Comparison of the added value of contrast-enhanced 3D fluid-attenuated inversion recovery and magnetization-prepared rapid acquisition of gradient echo sequences in relation to conventional postcontrast T1-weighted images for the evaluation of leptomening. Am J Neuroradiol2010; 31(5): 868–873.
29.
BonzanoLRoccatagliataLLevreroF, et al. In vitro investigation of poor cerebrospinal fluid suppression on fluid-attenuated inversion recovery images in the presence of a gadolinium-based contrast agent. Magn Reson Med2008; 60(1): 220–223.
30.
MamourianACHoopesPJLewisLD.Visualization of intravenously administered contrast material in the CSF on fluid-attenuated inversion-recovery MR images: An in vitro and animal-model investigation. Am J Neuroradiol2000; 21(1): 105–111.
31.
ZurawskiJTauhidSChuR, et al. 7T MRI cerebral leptomeningeal enhancement is common in relapsing-remitting multiple sclerosis and is associated with cortical and thalamic lesions. Mult Scler2020; 26(2): 177–187.
32.
OgawaRNakashimaITakahashiT, et al. MOG antibody-positive, benign, unilateral, cerebral cortical encephalitis with epilepsy. Neurol Neuroimmunol Neuroinflamm2017; 4(2): e322.
33.
BudhramAMirianALeC, et al. Unilateral cortical FLAIR-hyperintense lesions in anti-MOG-associated encephalitis with seizures (FLAMES): Characterization of a distinct clinico-radiographic syndrome. J Neurol2019; 266(10): 2481–2487.
34.
GardnerCMagliozziRDurrenbergerPF, et al. Cortical grey matter demyelination can be induced by elevated pro-inflammatory cytokines in the subarachnoid space of MOG-immunized rats. Brain2013; 136(Pt 12): 3596–3608.
