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Gadolinium-based MRI characterization of leptomeningeal inflammation in multiple sclerosis
Open accessAbstract
OBJECTIVE: To determine the frequency and nature of leptomeningeal contrast enhancement in multiple sclerosis (MS) via in vivo 3-tesla postcontrast T2-weighted, fluid-attenuated inversion recovery (FLAIR) MRI and 7-tesla postmortem MRI-pathology correlation. METHODS: Brain MRI, using the postcontrast T2-weighted, FLAIR technique, was prospectively collected in 299 MS cases and 37 age-matched neurologically healthy controls. Expert raters evaluated focal gadolinium enhancement in the leptomeningeal compartment. Two progressive MS cases came to autopsy after in vivo MRI characterization. Pathologic and immunohistochemical examination assessed the association of enhancement with leptomeningeal inflammation and adjacent cortical demyelination. RESULTS: Focal contrast enhancement was detected in the leptomeningeal compartment in 74 of 299 MS cases (25%) vs 1 of 37 neurologically healthy controls (2.7%; p = 0.001). Enhancement was nearly twice as frequent (p = 0.009) in progressive MS (39/118 cases, 33%) as in relapsing-remitting MS (35/181, 19%). Enhancing foci generally remained stable throughout the evaluation period (up to 5.5 years). Pathology showed perivascular lymphocytic and mononuclear infiltration in the enhancing areas in association with flanking subpial cortical demyelination. CONCLUSION: Leptomeningeal contrast enhancement occurs frequently in MS and is a noninvasive, in vivo marker of inflammation and associated subpial demyelination. It might therefore enable testing of new treatments aimed at eliminating this inflammation and potentially arresting progressive MS.
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“Similar considerations may hold with active leptomeningeal inflammation (Howell et al., 2011; Absinta et al., 2015).”
From A quantitative neuropathological assessment of translocator protein expression in multiple sclerosis (2019) · cites this paper as Absinta et al., 2015
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Zivadinov, R., Ramasamy, D. P., Hagemeier, J., Kolb, C., Bergsland, N., Schweser, F., Dwyer, M. G., Weinstock‐Guttman, B., & Hojnacki, D. W. (2018) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5541 · Cited by 49
“Therefore, we recommend using the subtraction approach for easier detection of LM CE mimics, such as meningeal blood vessels, large subarachnoid veins, and high signal intensity areas in regions adjacent to dural venous sinuses and basal meninges related to CSF enhancement.(9,10,12) In the present study of consecutive…”
ResultInfluentialMorgan, B. P., Gommerman, J. L., & Ramaglia, V. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.600656 · Cited by 51
“, 2020), emerging MRI approaches to identify and perhaps monitor the formation of TLT in patients (Absinta et al., 2015), and multi-dimensional technologies to phenotype cells in situ (Ramaglia et al.”
BackgroundInfluentialСергеевич, М. Г., Магонов, Е. П., Totolyan, N. A., Назаров, В. Д., Lapin, S. V., Маzing, A. V., Verbitskaya, E. V., Трофимова, Т. Н., Сергеевич, К. В., Shumilina, M. V., et al. (2017) · Neurology Research International · doi:10.1155/2017/8652463 · Cited by 47
“We showed in our study the LMCE frequency of 41%, which was higher than what had been published previously [9, 11].”
BackgroundResultInfluentialSerafini, B., Rosicarelli, B., Veroni, C., Zhou, L., Reali, C., & Aloisi, F. (2016) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlw063 · Cited by 46
“This concept is supported by the results of recent magnetic resonance imaging studies (12, 13).”
ResultBeyond focal cortical lesions in MS
Louapre, C., Govindarajan, S. T., Giannì, C., Langkammer, C., Sloane, J. A., Kinkel, R. P., & Mainero, C. (2015) · Neurology · doi:10.1212/wnl.0000000000002106 · Cited by 45
Freeze, W. M., Schnerr, R. S., Palm, W. M., Jansen, J. F., Jacobs, H. I., Hoff, E. I., Verhey, F. R., & Backes, W. H. (2017) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5273 · Cited by 43
“vious studies that used postcontrast FLAIR imaging reported pericortical gadolinium leakage that appears as signal enhancement in the CSF in various clinical disease conditions with BBB leakage, including acute ischemic stroke and MS.(8,9) The application of the postcontrast FLAIR technique has not yet been evaluated…”
BackgroundInfluentialBergsland, N., Ramasamy, D. P., Tavazzi, E., Hojnacki, D. W., Weinstock‐Guttman, B., & Zivadinov, R. (2019) · American Journal of Neuroradiology · doi:10.3174/ajnr.a6011 · Cited by 41
“LMCE foci were defined as signal intensity within the subarachnoid space that was substantially greater than that of brain parenchyma and characterized as being nodular, linear, or plate-like, as previously described.(11) All LMCE foci were confirmed in consensus by 2 experienced neuroimagers, each with 15 years of ex…”
BackgroundBeck, E., Gai, N., Filippini, S., Maranzano, J., Nair, G., & Reich, D. S. (2020) · Investigative Radiology · doi:10.1097/rli.0000000000000698 · Cited by 39
Self-citationEmerging Approaches for Validating and Managing Multiple Sclerosis Relapse
Mills, E. A., Mirza, A., & Mao‐Draayer, Y. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00116 · Cited by 41
“Advanced imaging techniques have also allowed for the detection of leptomeningeal inflammation, which in some cases has been pathologically confirmed to be both associated with follicular structures and in close proximity to subpial demyelinating lesions (15).”
BackgroundCommon Clinical and Imaging Conditions Misdiagnosed as Multiple Sclerosis
Sıva, A. (2017) · Neurologic Clinics · doi:10.1016/j.ncl.2017.08.014 · Cited by 43
Leptomeningeal inflammation in multiple sclerosis: Insights from animal and human studies
Wicken, C., Nguyen, J. V., Karna, R., & Bhargava, P. (2018) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2018.09.025 · Cited by 40
Central Vein Sign Profile of Newly Developing Lesions in Multiple Sclerosis
Al‐Louzi, O., Letchuman, V., Manukyan, S., Beck, E., Roy, S., Ohayon, J. M., Pham, D. L., Cortese, I. C. M., Sati, P., & Reich, D. S. (2022) · Neurology Neuroimmunology & Neuroinflammation · doi:10.1212/nxi.0000000000001120 · Cited by 41
Self-citationÖzütemiz, C., White, M., Elvendahl, W., Eryaman, Y., Marjańska, M., Metzger, G. J., Patriat, R., Kulesa, J., Harel, N., Watanabe, Y., et al. (2023) · American Journal of Roentgenology · doi:10.2214/ajr.23.29342 · Cited by 39
Shan, K., Pang, R., Zhao, C., Liu, X., Gao, W., Zhang, J., Zhao, D., Wang, Y., & Qiu, W. (2017) · Cellular and Molecular Immunology · doi:10.1038/cmi.2017.12 · Cited by 39
Jonas, S. N., Izbudak, I., Frazier, A. A., & Harrison, D. M. (2018) · American Journal of Neuroradiology · doi:10.3174/ajnr.a5796 · Cited by 39
“1804 Jonas Oct 2018 www.ajnr.org important new insight into the longitudinal activity of meningeal enhancement in MS.”
BackgroundResultInfluentialJakimovski, D., Ramanathan, M. K., Weinstock‐Guttman, B., Bergsland, N., Ramasamay, D. P., Carl, E. M., Dwyer, M. G., & Zivadinov, R. (2019) · Multiple Sclerosis Journal · doi:10.1177/1352458519828667 · Cited by 39
Aseptic meningitis and leptomeningeal enhancement associated with anti-MOG antibodies: A review
Gombolay, G. Y., & Gadde, J. A. (2021) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2021.577653 · Cited by 39
Role of B cells and antibodies in multiple sclerosis
Wanleenuwat, P., & Iwanowski, P. S. (2019) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2019.101416 · Cited by 40
MRI in multiple sclerosis: clinical and research update
Inglese, M., & Petracca, M. (2018) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000559 · Cited by 37
Contribution of B cells to cortical damage in multiple sclerosis
Bhargava, P., Hartung, H.-P., & Calabresi, P. A. (2022) · Brain · doi:10.1093/brain/awac233 · Cited by 36
Self-citationLin, J.-P., Brake, A., Donadieu, M., Lee, A., Smith, G., Hu, K., Nair, G., Kawaguchi, R., Sati, P., Geschwind, D. H., et al. (2025) · Science · doi:10.1126/science.adp6325 · Cited by 35
Self-citationWang, A. A., Luessi, F., Neziraj, T., Pössnecker, E., Zuo, M., Engel, S., Hanuscheck, N., Florescu, A., Bugbee, E., Xianjie, I., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adi0295 · Cited by 37
Impact of Glatiramer Acetate on B Cell-Mediated Pathogenesis of Multiple Sclerosis
Küerten, S., Jackson, L. J., Kaye, J., & Vollmer, T. L. (2018) · CNS Drugs · doi:10.1007/s40263-018-0567-8 · Cited by 35
Imaging Mechanisms of Disease Progression in Multiple Sclerosis: Beyond Brain Atrophy
Bagnato, F. R., Gauthier, S. A., Laule, C., Moore, G. R. W., Bove, R. M., Cai, Z., Cohen‐Adad, J., Harrison, D. M., Klawiter, E. C., Morrow, S. A., et al. (2020) · Journal of Neuroimaging · doi:10.1111/jon.12700 · Cited by 37
Self-citationRovira, À., Doniselli, F. M., Auger, C., Haider, L., Hodel, J., Severino, M., Wattjes, M. P., van der Molen, A. J., Jasperse, B., Mallio, C. A., et al. (2023) · European Radiology · doi:10.1007/s00330-023-10151-y · Cited by 35
“Additionally, this post-contrast T2-FLAIR may be helpful to detect areas of leptomeningeal enhancement, an imaging feature that has emerged as a surrogate imaging marker of current or prior leptomeningeal inflammation and linked to cortical damage [58, 59].”
MRI in multiple sclerosis: what is changing?
Filippi, M., Preziosa, P., & Rocca, M. A. (2018) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000572 · Cited by 33
CSF enhancement on post-contrast fluid-attenuated inversion recovery images; a systematic review
Freeze, W. M., van der Thiel, M., de Bresser, J., Klijn, C. J. M., van Etten, E. S., Jansen, J. F. A., van der Weerd, L., Jacobs, H. I. L., Backes, W. H., & van Veluw, S. J. (2020) · NeuroImage: Clinical · doi:10.1016/j.nicl.2020.102456 · Cited by 33
“…of neuroradiological mimics of GBCA enhancement in the CSF space (Stuckey et al., 2007), including enhancement in or near dural venous sinuses (Absinta, 2017, 2015; Harrison, 2017; Absinta, et al., 2017), basal meninges or large subarachnoid veins (Absinta, 2017, 2015; Harrison, 2017),…”
BackgroundMethodResultInfluentialGroppa, S., González‐Escamilla, G., Eshaghi, A., Meuth, S. G., & Ciccarelli, O. (2021) · Brain Communications · doi:10.1093/braincomms/fcab237 · Cited by 34
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“with MS studies showing mostly supratentorial and uni- or bifocal lesions.(27,28)”
BackgroundAbnormalities in normal-appearing white matter from which multiple sclerosis lesions arise
Elliott, C., MomayyezSiahkal, P., Arnold, D. L., Liu, D., Ke, J., Zhu, L., Zhu, B. Y., George, I. C., Bradley, D. P., Fisher, E., et al. (2021) · Brain Communications · doi:10.1093/braincomms/fcab176 · Cited by 33
The Role of Advanced Magnetic Resonance Imaging Techniques in Multiple Sclerosis Clinical Trials
Mahajan, K. R., & Ontaneda, D. (2017) · Neurotherapeutics · doi:10.1007/s13311-017-0561-8 · Cited by 34
“Although LME occurs in 25% [269, 270] of patients with MS, it is not specific.”
BackgroundAge-dependent gray matter demyelination is associated with leptomeningeal neutrophil accumulation
Zuo, M., Fettig, N. M., Bernier, L., Pössnecker, E., Spring, S., Pu, A., Xianjie, I., Lee, D. S., Ward, L. A., Sharma, A. K., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.158144 · Cited by 31
Ocrelizumab: a B-cell depleting therapy for multiple sclerosis
Jakimovski, D., Weinstock‐Guttman, B., Ramanathan, M. K., Kolb, C., Hojnacki, D. W., Minagar, A., & Zivadinov, R. (2017) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2017.1347632 · Cited by 31
MRI biomarkers of disease progression and conversion to secondary-progressive multiple sclerosis
Tavazzi, E., Zivadinov, R., Dwyer, M. G., Jakimovski, D., Singhal, T., Weinstock‐Guttman, B., & Bergsland, N. (2020) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2020.1757435 · Cited by 33
Magnetic Resonance Imaging in Primary Progressive Multiple Sclerosis Patients
Siger, M. (2022) · Clinical Neuroradiology · doi:10.1007/s00062-022-01144-3 · Cited by 32
“Using 3D postcontrast T2 FLAIR imaging, it is possible to detect more LME in MS patients compared to conventional T1-weighted imaging [37].”
MethodWen, J., Yablonskiy, D. A., Luo, J., Lancia, S., Hildebolt, C. F., & Cross, A. H. (2015) · NeuroImage Clinical · doi:10.1016/j.nicl.2015.08.003 · Cited by 30
“…et al., 2013; Derakhshan et al., 2014a, 2014b; Schmierer et al., 2010; Seewann et al., 2011; Yarnykh et al., 2015) and transverse relaxation rate related measurement at ultra-high field (Absinta et al., 2015; Mainero et al., 2015), have been used to improve the detection of cortical MS damage.”
MethodNew Prospects for Ultra-High-Field Magnetic Resonance Imaging in Multiple Sclerosis
Ineichen, B. V., Beck, E., Piccirelli, M., & Reich, D. S. (2021) · Investigative Radiology · doi:10.1097/rli.0000000000000804 · Cited by 30
Self-citation
Metadata
- Authors
- Absinta, M., Vuolo, L., Rao, A., Nair, G., Sati, P., Cortese, I. C. M., Ohayon, J., Fenton, K., Reyes-Mantilla, M. I., Maric, D., Calabresi, P. A., Butman, J. A., Pardo, C. A., & Reich, D. S.
- Affiliations
- National Institutes of Health (US)
- From the Translational Neuroradiology Unit (M.A., L.V., A.R., G.N., P.S., D.S.R.), Neuroimmunology Clinic (I.C.M.C., J.O., K.F.), and Flow Cytometry Core Facility (D.M.), National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD; Neuroimaging Research Unit (M.A.), Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan; Department of Neurology and Radiology (L.V.), University of Florence, Italy;...
- ORCID
- Venue
- Neurology
- Published
- 2015-07-07
- Volume
- 85
- Issue
- 1
- Pages
- 18-28
- ISSN
- 0028-3878 (ISSN-L)
- 1526-632X
- PMC
- PMC4501940
- OpenAlex
- W2169159041
- Cited by
- 296
- References
- 36
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 32 · 2023: 30 · 2022: 27 · 2021: 32 · 2020: 32 · 2019: 31 · 2018: 28 · 2017: 27 · 2016: 26 · 2015: 6
- FWCI
- 23.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neurology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke
- Topics
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Health Sciences › Medicine › Oncology › Polyomavirus and related diseases
- Keywords
- multiple sclerosis, leptomeningeal inflammation, gadolinium-enhancing lesions, progressive multiple sclerosis, relapsing-remitting multiple sclerosis, perivascular lymphocytic infiltrate, cortical demyelination, MRI-pathology correlation, 7T MRI
- MeSH terms
- Gadolinium, Humans, Magnetic Resonance Imaging, Meninges, Meningitis, Multiple Sclerosis, Relapsing-Remitting
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