Choroid plexus volume changes in multiple sclerosis: insights from a systematic review and meta-analysis of magnetic resonance imaging studies.
Choroid plexus
MRI
Meta-analysis
Multiple sclerosis
Neuro-inflammation
Systematic review
Journal
Neuroradiology
ISSN: 1432-1920
Titre abrégé: Neuroradiology
Pays: Germany
ID NLM: 1302751
Informations de publication
Date de publication:
06 Aug 2024
06 Aug 2024
Historique:
received:
29
04
2024
accepted:
27
07
2024
medline:
6
8
2024
pubmed:
6
8
2024
entrez:
6
8
2024
Statut:
aheadofprint
Résumé
Multiple sclerosis (MS) is a chronic autoimmune disease characterized by the destruction of the myelin sheath within the central nervous system. The etiology of MS involves a complex interplay of genetic, environmental, and immunological factors. Recent studies indicated the potential role of the choroid plexus (CP) in the pathogenesis and progression of MS. This systematic review aims to assess existing research on the volume alterations of the CP in MS patients compared to the normal population. A comprehensive search was conducted across databases including PubMed, Embase, Scopus, and Web of Science up to June 2024. Data from the included studies were synthesized using a meta-analytical approach with a random-effects model, assessing heterogeneity with the I We included 17 studies in this systematic review. The meta-analysis, which included data from eight studies reporting CP volume relative to TIV, found a statistically significant increase in CP volume in MS patients compared to healthy controls (HCs). The SMD was 0.77 (95% CI: 0.61 to 0.93), indicating a large effect size. This analysis showed no heterogeneity (I² = 0%). A separate meta-analysis was conducted using five studies that reported CP volume as normalized volume, resulting in an SMD of 0.63 (95% CI: 0.2-1.06). This study demonstrates an increase in CP volume among MS patients compared to HCs, implying the potential involvement of CP in MS pathogenesis and/or progression. These results show that CP might serve as a radiological indicator in the diagnosis and prognosis of MS.
Identifiants
pubmed: 39105769
doi: 10.1007/s00234-024-03439-3
pii: 10.1007/s00234-024-03439-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Thompson AJ, Baranzini SE, Geurts J, Hemmer B, Ciccarelli O (2018) Multiple sclerosis. Lancet 391:1622–1636. https://doi.org/10.1016/s0140-6736(18)30481-1
doi: 10.1016/s0140-6736(18)30481-1
pubmed: 29576504
Compston A, Coles A (2008) Multiple sclerosis. Lancet 372:1502–1517. https://doi.org/10.1016/s0140-6736(08)61620-7
doi: 10.1016/s0140-6736(08)61620-7
pubmed: 18970977
Kobelt G, Thompson A, Berg J, Gannedahl M, Eriksson J (2017) New insights into the burden and costs of multiple sclerosis in Europe. Mult Scler 23:1123–1136. https://doi.org/10.1177/1352458517694432
doi: 10.1177/1352458517694432
pubmed: 28273775
pmcid: 5476197
Orton SM, Herrera BM, Yee IM, Valdar W, Ramagopalan SV, Sadovnick AD, Ebers GC (2006) Sex ratio of multiple sclerosis in Canada: a longitudinal study. Lancet Neurol 5:932–936. https://doi.org/10.1016/s1474-4422(06)70581-6
doi: 10.1016/s1474-4422(06)70581-6
pubmed: 17052660
Baecher-Allan C, Kaskow BJ, Weiner HL (2018) Multiple sclerosis: mechanisms and immunotherapy. Neuron 97:742–768. https://doi.org/10.1016/j.neuron.2018.01.021
doi: 10.1016/j.neuron.2018.01.021
pubmed: 29470968
Mihaljevic S, Michalicova A, Bhide M, Kovac A (2021) Pathophysiology of the choroid plexus in brain diseases. Gen Physiol Biophys 40:443–462. https://doi.org/10.4149/gpb_2021032
doi: 10.4149/gpb_2021032
pubmed: 34897020
Johanson CE, Duncan JA, Klinge PM, Brinker T, Stopa EG, Silverberg GD (2008) Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res 5. https://doi.org/10.1186/1743-8454-5-10
Spector R, Keep RF, Snodgrass R, Smith S, Q.R., and, Johanson CE (2015) A balanced view of choroid plexus structure and function: focus on adult humans. Exp Neurol 267:78–86. https://doi.org/10.1016/j.expneurol.2015.02.032
doi: 10.1016/j.expneurol.2015.02.032
pubmed: 25747036
Kratzer I, Ek J, Stolp H (2020) The molecular anatomy and functions of the choroid plexus in healthy and diseased brain. Biochim Biophys Acta Biomembr 1862:183430. https://doi.org/10.1016/j.bbamem.2020.183430
doi: 10.1016/j.bbamem.2020.183430
pubmed: 32750317
Rodriguez-Mogeda C, Rodríguez-Lorenzo S, Attia J, van Horssen J, Witte ME, de Vries HE (2022) Breaching brain barriers: B Cell Migration in multiple sclerosis. Biomolecules 12. https://doi.org/10.3390/biom12060800
Kaur C, Rathnasamy G, Ling EA (2016) The Choroid Plexus in healthy and diseased brain. J Neuropathol Exp Neurol 75:198–213. https://doi.org/10.1093/jnen/nlv030
doi: 10.1093/jnen/nlv030
pubmed: 26888305
Marques F, Sousa JC (2015) The choroid plexus is modulated by various peripheral stimuli: implications to diseases of the central nervous system. Front Cell Neurosci 9:136. https://doi.org/10.3389/fncel.2015.00136
doi: 10.3389/fncel.2015.00136
pubmed: 26236190
pmcid: 4394702
Dendrou CA, Fugger L, Friese MA (2015) Immunopathology of multiple sclerosis. Nat Rev Immunol 15:545–558. https://doi.org/10.1038/nri3871
doi: 10.1038/nri3871
pubmed: 26250739
Liu Z, Pardini M, Yaldizli Ö, Sethi V, Muhlert N, Wheeler-Kingshott CA, Samson RS, Miller DH, Chard DT (2015) Magnetization transfer ratio measures in normal-appearing white matter show periventricular gradient abnormalities in multiple sclerosis. Brain 138:1239–1246. https://doi.org/10.1093/brain/awv065
doi: 10.1093/brain/awv065
pubmed: 25823475
pmcid: 5963416
Poirion E, Tonietto M, Lejeune FX, Ricigliano VAG, Boudot de la Motte M, Benoit C, Bera G, Kuhnast B, Bottlaender M, Bodini B, Stankoff B (2021) Structural and clinical correlates of a Periventricular gradient of Neuroinflammation in multiple sclerosis. Neurology 96:e1865–e1875. https://doi.org/10.1212/wnl.0000000000011700
doi: 10.1212/wnl.0000000000011700
pubmed: 33737372
pmcid: 8105971
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71
doi: 10.1136/bmj.n71
pubmed: 33782057
pmcid: 8005924
Kurtzke JF (1983) 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
doi: 10.1212/wnl.33.11.1444
pubmed: 6685237
McArthur A, Klugarová J, Yan H, Florescu S (2020) Chapter 4: Systematic Reviews of Text and Opinion. In. https://doi.org/10.46658/JBIMES-20-05
de Deus Vieira G, Antônio FF, Damasceno A (2024) Enlargement of the choroid plexus in pediatric multiple sclerosis. Neuroradiology 66:1199–1202. https://doi.org/10.1007/s00234-024-03366-3
doi: 10.1007/s00234-024-03366-3
pubmed: 38668802
Fleischer V, Gonzalez-Escamilla G, Ciolac D, Albrecht P, Küry P, Gruchot J, Dietrich M, Hecker C, Müntefering T, Bock S et al (2021) Translational value of choroid plexus imaging for tracking neuroinflammation in mice and humans. Proc Natl Acad Sci U S A 118. https://doi.org/10.1073/pnas.2025000118
Müller J, Sinnecker T, Wendebourg MJ, Schläger R, Kuhle J, Schädelin S, Benkert P, Derfuss T, Cattin P, Jud C et al (2022) Choroid Plexus Volume in Multiple Sclerosis vs Neuromyelitis Optica Spectrum Disorder: A Retrospective, Cross-sectional Analysis. Neurol Neuroimmunol Neuroinflamm 9. https://doi.org/10.1212/nxi.0000000000001147
Bergsland N, Dwyer MG, Jakimovski D, Tavazzi E, Benedict RHB, Weinstock-Guttman B, Zivadinov R (2023) Association of Choroid Plexus Inflammation on MRI with clinical disability progression over 5 years in patients with multiple sclerosis. Neurology 100:e911–e920. https://doi.org/10.1212/wnl.0000000000201608
doi: 10.1212/wnl.0000000000201608
pubmed: 36543575
pmcid: 9990433
Margoni M, Gueye M, Meani A, Pagani E, Moiola L, Preziosa P, Filippi M, Rocca MA (2023) Choroid plexus enlargement in paediatric multiple sclerosis: clinical relevance and effect of sex. J Neurol Neurosurg Psychiatry 94:181–188. https://doi.org/10.1136/jnnp-2022-330343
doi: 10.1136/jnnp-2022-330343
pubmed: 36351790
Storelli L, Pagani E, Rubin M, Margoni M, Filippi M, Rocca MA (2023) A fully automatic method to Segment Choroid plexuses in multiple sclerosis using conventional MRI sequences. J Magn Reson Imaging. https://doi.org/10.1002/jmri.28937
doi: 10.1002/jmri.28937
pubmed: 37530734
Preziosa P, Pagani E, Meani A, Storelli L, Margoni M, Yudin Y, Tedone N, Biondi D, Rubin M, Rocca MA, Filippi M (2024) Chronic active lesions and larger choroid plexus explain cognition and fatigue in multiple sclerosis. Neurol Neuroimmunol Neuroinflamm 11:e200205. https://doi.org/10.1212/nxi.0000000000200205
doi: 10.1212/nxi.0000000000200205
pubmed: 38350048
pmcid: 11073888
Akaishi T, Fujimori J, Nakashima I (2024) Enlarged choroid plexus in multiple sclerosis is associated with increased lesion load and atrophy in white matter but not gray matter atrophy. Mult Scler Relat Disord 82:105424. https://doi.org/10.1016/j.msard.2024.105424
doi: 10.1016/j.msard.2024.105424
pubmed: 38181695
Ricigliano VAG, Louapre C, Poirion E, Colombi A, Yazdan Panah A, Lazzarotto A, Morena E, Martin E, Bottlaender M, Bodini B, Seilhean D, Stankoff B (2022) Imaging characteristics of Choroid Plexuses in Presymptomatic multiple sclerosis: a retrospective study. Neurol Neuroimmunol Neuroinflamm 9. https://doi.org/10.1212/nxi.0000000000200026
Ricigliano VAG, Morena E, Colombi A, Tonietto M, Hamzaoui M, Poirion E, Bottlaender M, Gervais P, Louapre C, Bodini B, Stankoff B (2021) Choroid Plexus Enlargement in Inflammatory multiple sclerosis: 3.0-T MRI and translocator protein PET evaluation. Radiology 301:166–177. https://doi.org/10.1148/radiol.2021204426
doi: 10.1148/radiol.2021204426
pubmed: 34254858
Klistorner S, Barnett MH, Parratt J, Yiannikas C, Graham SL, Klistorner A (2022) Choroid plexus volume in multiple sclerosis predicts expansion of chronic lesions and brain atrophy. Ann Clin Transl Neurol 9:1528–1537. https://doi.org/10.1002/acn3.51644
doi: 10.1002/acn3.51644
pubmed: 36056634
pmcid: 9539382
Wang X, Zhu Q, Yan Z, Shi Z, Xu Y, Liu Y, Li Y (2023) Enlarged choroid plexus related to iron rim lesions and deep gray matter atrophy in relapsing-remitting multiple sclerosis. Mult Scler Relat Disord 75:104740. https://doi.org/10.1016/j.msard.2023.104740
doi: 10.1016/j.msard.2023.104740
pubmed: 37146422
Klistorner S, Van der Walt A, Barnett MH, Butzkueven H, Kolbe S, Parratt J, Yiannikas C, Klistorner A (2023) Choroid plexus volume is enlarged in clinically isolated syndrome patients with optic neuritis. Mult Scler 29:540–548. https://doi.org/10.1177/13524585231157206
doi: 10.1177/13524585231157206
pubmed: 36876595
Raghib MF, Bao F, Elkhooly M, Bernitsas E (2024) Choroid plexus volume as a marker of retinal atrophy in relapsing remitting multiple sclerosis. J Neurol Sci 457:122884. https://doi.org/10.1016/j.jns.2024.122884
doi: 10.1016/j.jns.2024.122884
pubmed: 38237367
Xie Y, Zhu H, Yao Y, Liu C, Wu S, Zhang Y, Zhu W (2024) Enlarged choroid plexus in relapsing-remitting multiple sclerosis may lead to brain structural changes through the glymphatic impairment. Multiple Sclerosis and Related Disorders 85. https://doi.org/10.1016/j.msard.2024.105550
Chen X, Luo D, Zheng Q, Peng Y, Han Y, Luo Q, Zhu Q, Luo T, Li Y (2023) Enlarged choroid plexus related to cortical atrophy in multiple sclerosis. Eur Radiol 33:2916–2926. https://doi.org/10.1007/s00330-022-09277-2
doi: 10.1007/s00330-022-09277-2
pubmed: 36547675
Jankowska A, Chwojnicki K, Grzywińska M, Trzonkowski P, Szurowska E (2023) Choroid Plexus volume Change—A candidate for a new Radiological marker of MS Progression. Diagnostics 13. https://doi.org/10.3390/diagnostics13162668
Andrade C (2020) Mean difference, standardized Mean difference (SMD), and their use in Meta-Analysis: as simple as it gets. J Clin Psychiatry 81. https://doi.org/10.4088/JCP.20f13681
Solár P, Zamani A, Kubíčková L, Dubový P, Joukal M (2020) Choroid plexus and the blood-cerebrospinal fluid barrier in disease. Fluids Barriers CNS 17:35. https://doi.org/10.1186/s12987-020-00196-2
doi: 10.1186/s12987-020-00196-2
pubmed: 32375819
pmcid: 7201396
Graumann U, Reynolds R, Steck AJ, Schaeren-Wiemers N (2003) Molecular changes in normal appearing white matter in multiple sclerosis are characteristic of neuroprotective mechanisms against hypoxic insult. Brain Pathol 13:554–573. https://doi.org/10.1111/j.1750-3639.2003.tb00485.x
doi: 10.1111/j.1750-3639.2003.tb00485.x
pubmed: 14655760
Rodríguez-Lorenzo S, Ferreira Francisco DM, Vos R, van Het Hof B, Rijnsburger M, Schroten H, Ishikawa H, Beaino W, Bruggmann R, Kooij G, de Vries HE (2020) Altered secretory and neuroprotective function of the choroid plexus in progressive multiple sclerosis. Acta Neuropathol Commun 8:35. https://doi.org/10.1186/s40478-020-00903-y
doi: 10.1186/s40478-020-00903-y
pubmed: 32192527
pmcid: 7083003
Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R, Puopolo M, Reynolds R, Aloisi F (2007) Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 130:1089–1104. https://doi.org/10.1093/brain/awm038
doi: 10.1093/brain/awm038
pubmed: 17438020
Cencioni MT, Mattoscio M, Magliozzi R, Bar-Or A, Muraro PA (2021) B cells in multiple sclerosis - from targeted depletion to immune reconstitution therapies. Nat Rev Neurol 17:399–414. https://doi.org/10.1038/s41582-021-00498-5
doi: 10.1038/s41582-021-00498-5
pubmed: 34075251
Haas J, Bekeredjian-Ding I, Milkova M, Balint B, Schwarz A, Korporal M, Jarius S, Fritz B, Lorenz HM, Wildemann B (2011) B cells undergo unique compartmentalized redistribution in multiple sclerosis. J Autoimmun 37:289–299. https://doi.org/10.1016/j.jaut.2011.08.003
doi: 10.1016/j.jaut.2011.08.003
pubmed: 21924866
Haas J, Rudolph H, Costa L, Faller S, Libicher S, Würthwein C, Jarius S, Ishikawa H, Stump-Guthier C, Tenenbaum T et al (2020) The Choroid Plexus is permissive for a Preactivated Antigen-experienced memory B-Cell subset in multiple sclerosis. Front Immunol 11:618544. https://doi.org/10.3389/fimmu.2020.618544
doi: 10.3389/fimmu.2020.618544
pubmed: 33574821
Muthuraman M, Oshaghi M, Fleischer V, Ciolac D, Othman A, Meuth SG, Gonzalez-Escamilla G, Groppa S (2023) Choroid plexus imaging to track neuroinflammation - a translational model for mouse and human studies. Neural Regen Res 18:521–522. https://doi.org/10.4103/1673-5374.346471
doi: 10.4103/1673-5374.346471
pubmed: 36018158
Fadda G, Brown RA, Magliozzi R, Aubert-Broche B, O’Mahony J, Shinohara RT, Banwell B, Marrie RA, Yeh EA, Collins DL, Arnold DL, Bar-Or A (2019) A surface-in gradient of thalamic damage evolves in pediatric multiple sclerosis. Ann Neurol 85:340–351. https://doi.org/10.1002/ana.25429
doi: 10.1002/ana.25429
pubmed: 30719730
pmcid: 6593844
Lassmann H (2005) Multiple sclerosis pathology: evolution of pathogenetic concepts. Brain Pathol 15:217–222. https://doi.org/10.1111/j.1750-3639.2005.tb00523.x
doi: 10.1111/j.1750-3639.2005.tb00523.x
pubmed: 16196388
Tonietto M, Poirion E, Lazzarotto A, Ricigliano V, Papeix C, Bottlaender M, Bodini B, Stankoff B (2023) Periventricular remyelination failure in multiple sclerosis: a substrate for neurodegeneration. Brain 146:182–194. https://doi.org/10.1093/brain/awac334
doi: 10.1093/brain/awac334
pubmed: 36097347
Hablitz LM, Nedergaard M (2021) The Glymphatic System: a Novel Component of Fundamental Neurobiology. J Neurosci 41:7698–7711. https://doi.org/10.1523/jneurosci.0619-21.2021
doi: 10.1523/jneurosci.0619-21.2021
pubmed: 34526407
pmcid: 8603752