Decreased DTI-ALPS and choroid plexus enlargement in fibromyalgia: a preliminary multimodal MRI study.
Choroid plexus
Diffusion tensor imaging along the perivascular space
Fibromyalgia
Glymphatic system
Journal
Neuroradiology
ISSN: 1432-1920
Titre abrégé: Neuroradiology
Pays: Germany
ID NLM: 1302751
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
06
08
2023
accepted:
09
10
2023
medline:
17
11
2023
pubmed:
23
10
2023
entrez:
23
10
2023
Statut:
ppublish
Résumé
The glymphatic system is a fluid exchange pathway that clears waste products that is crucial for the maintenance of brain homeostasis. However, the exact role it plays in the emergence of fibromyalgia (FM) is still not fully understood. Here, we explored the changes in non-invasive MRI proxy probably related to the glymphatic function in FM patients, and explored brain-behavior relationships. A total of 40 participants, consisting of 20 individuals with FM and 20 healthy controls (HCs), were included in the study. The participants underwent structural T1-weighted MRI, diffusion tensor imaging (DTI), and clinical assessment. The data was obtained from an open access dataset. The study compared non-invasive MRI indices, including choroid plexus (CP) volume and DTI analysis along the perivascular space (ALPS), between the FM and HC groups. Furthermore, correlation analysis was conducted to determine the correlation between clinical parameters and both CP volume and DTI-ALPS index. Patients with FM had significantly higher CP volume and a lower DTI-ALPS index than HCs adjusting for age and intracranial volume. Higher CP volume was associated with lower DTI-ALPS index, and longer disease duration. Our findings demonstrate aberrant glymphatic function in FM, and that dysfunction in the brain glymphatic system may play a role in the neural mechanisms underlying FM.
Identifiants
pubmed: 37870589
doi: 10.1007/s00234-023-03240-8
pii: 10.1007/s00234-023-03240-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1749-1755Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Clauw DJ (2014) Fibromyalgia: a clinical review. JAMA 311:1547–1555
doi: 10.1001/jama.2014.3266
pubmed: 24737367
Harte SE, Clauw DJ, Hayes JM, Feldman EL, St Charles IC, Watson CJ (2017) Reduced intraepidermal nerve fiber density after a sustained increase in insular glutamate: a proof-of-concept study examining the pathogenesis of small fiber pathology in fibromyalgia. Pain Rep 2:e590
doi: 10.1097/PR9.0000000000000590
pubmed: 29392206
pmcid: 5741296
Kaplan CM, Schrepf A, Ichesco E, Larkin T, Harte SE, Harris RE, Murray AD, Waiter GD, Clauw DJ, Basu N (2020) Association of inflammation with pronociceptive brain connections in rheumatoid arthritis patients with concomitant fibromyalgia. Arthritis Rheumatol 72:41–46
doi: 10.1002/art.41069
pubmed: 31379121
Kosek E, Cohen M, Baron R, Gebhart GF, Mico JA, Rice ASC, Rief W, Sluka AK (2016) Do we need a third mechanistic descriptor for chronic pain states? Pain 157:1382–1386
doi: 10.1097/j.pain.0000000000000507
pubmed: 26835783
Harris RE, Sundgren PC, Craig AD, Kirshenbaum E, Sen A, Napadow V, Clauw DJ (2009) Elevated insular glutamate in fibromyalgia is associated with experimental pain. Arthritis Rheum 60:3146–3152
doi: 10.1002/art.24849
pubmed: 19790053
pmcid: 2827610
Foerster BR, Petrou M, Edden RA, Sundgren PC, Schmidt-Wilcke T, Lowe SE, Harte SE, Clauw DJ, Harris RE (2012) Reduced insular gamma-aminobutyric acid in fibromyalgia. Arthritis Rheum 64:579–583
doi: 10.1002/art.33339
pubmed: 21913179
pmcid: 3374930
Pomares FB, Roy S, Funck T, Feier NA, Thiel A, Fitzcharles MA, Schweinhardt P (2020) Upregulation of cortical GABAA receptor concentration in fibromyalgia. Pain 161:74–82
doi: 10.1097/j.pain.0000000000001707
pubmed: 31569142
Harper DE, Ichesco E, Schrepf A, Hampson JP, Clauw DJ, Schmidt-Wilcke T, Harris RE, Harte SE (2018) Resting functional connectivity of the periaqueductal gray is associated with normal inhibition and pathological facilitation in conditioned pain modulation. J Pain 19:631–635 (e615)
doi: 10.1016/j.jpain.2018.01.001
Jessen NA, Munk AS, Lundgaard I, Nedergaard M (2015) The glymphatic system: a beginner’s guide. Neurochem Res 40:2583–2599
doi: 10.1007/s11064-015-1581-6
pubmed: 25947369
pmcid: 4636982
Rasmussen MK, Mestre H, Nedergaard M (2018) The glymphatic pathway in neurological disorders. Lancet Neurol 17:1016–1024
doi: 10.1016/S1474-4422(18)30318-1
pubmed: 30353860
pmcid: 6261373
Bae YJ, Kim JM, Choi BS, Ryoo N, Song YS, Nam Y, Yoon IY, Cho SJ, Kim JH (2023) Altered brain glymphatic flow at diffusion-tensor MRI in rapid eye movement sleep behavior disorder. Radiology 307:e221848
doi: 10.1148/radiol.221848
pubmed: 37158722
Hsu JL, Wei YC, Toh CH, Hsiao IT, Lin KJ, Yen TC, Liao MF, Ro LS (2023) Magnetic resonance images implicate that glymphatic alterations mediate cognitive dysfunction in Alzheimer disease. Ann Neurol 93:164–174
doi: 10.1002/ana.26516
pubmed: 36214568
Carotenuto A, Cacciaguerra L, Pagani E, Preziosa P, Filippi M, Rocca MA (2022) Glymphatic system impairment in multiple sclerosis: relation with brain damage and disability. Brain 145:2785–2795
doi: 10.1093/brain/awab454
pubmed: 34919648
Li Y, Han H, Shi K, Cui D, Yang J, Alberts IL, Yuan L, Zhao G, Wang R, Cai X, Teng Z (2020) The mechanism of downregulated interstitial fluid drainage following neuronal excitation. Aging Dis 11:1407–1422
doi: 10.14336/AD.2020.0224
pubmed: 33269097
pmcid: 7673848
Goldman N, Hablitz LM, Mori Y, Nedergaard M (2020) The glymphatic system and pain. Med Acupunct 32:373–376
doi: 10.1089/acu.2020.1489
pubmed: 33362890
pmcid: 7755843
Sarzi-Puttini P, Giorgi V, Marotto D, Atzeni F (2020) Fibromyalgia: an update on clinical characteristics, aetiopathogenesis and treatment. Nat Rev Rheumatol 16:645–660
doi: 10.1038/s41584-020-00506-w
pubmed: 33024295
Taoka T, Masutani Y, Kawai H, Nakane T, Matsuoka K, Yasuno F, Kishimoto T, Naganawa S (2017) Evaluation of glymphatic system activity with the diffusion MR technique: diffusion tensor image analysis along the perivascular space (DTI-ALPS) in Alzheimer’s disease cases. Jpn J Radiol 35:172–178
doi: 10.1007/s11604-017-0617-z
pubmed: 28197821
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
doi: 10.1212/WNL.0000000000201608
pubmed: 36543575
pmcid: 9990433
Tadayon E, Pascual-Leone A, Press D, Santarnecchi E, Alzheimer’s Disease Neuroimaging I, (2020) Choroid plexus volume is associated with levels of CSF proteins: relevance for Alzheimer’s and Parkinson’s disease. Neurobiol Aging 89:108–117
doi: 10.1016/j.neurobiolaging.2020.01.005
pubmed: 32107064
pmcid: 9094632
Garcia Campayo J, Rodero B, Alda M, Sobradiel N, Montero J, Moreno S (2008) Validation of the Spanish version of the Pain Catastrophizing Scale in fibromyalgia. Med Clin (Barc) 131:487–492
pubmed: 19007576
Kendall PC, Finch AJ Jr, Auerbach SM, Hooke JF, Mikulka PJ (1976) The State-Trait Anxiety Inventory: a systematic evaluation. J Consult Clin Psychol 44:406–412
doi: 10.1037/0022-006X.44.3.406
pubmed: 932270
Smarr KL, Keefer AL (2011) Measures of depression and depressive symptoms: Beck Depression Inventory-II (BDI-II), Center for Epidemiologic Studies Depression Scale (CES-D), Geriatric Depression Scale (GDS), Hospital Anxiety and Depression Scale (HADS), and Patient Health Questionnaire-9 (PHQ-9). Arthritis Care Res (Hoboken) 63(Suppl 11):S454-466
pubmed: 22588766
Veraart J, Novikov DS, Christiaens D, Ades-Aron B, Sijbers J, Fieremans E (2016) Denoising of diffusion MRI using random matrix theory. Neuroimage 142:394–406
doi: 10.1016/j.neuroimage.2016.08.016
pubmed: 27523449
Kellner E, Dhital B, Kiselev VG, Reisert M (2016) Gibbs-ringing artifact removal based on local subvoxel-shifts. Magn Reson Med 76:1574–1581
doi: 10.1002/mrm.26054
pubmed: 26745823
Andersson JLR, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125:1063–1078
doi: 10.1016/j.neuroimage.2015.10.019
pubmed: 26481672
Tournier JD, Smith R, Raffelt D, Tabbara R, Dhollander T, Pietsch M, Christiaens D, Jeurissen B, Yeh CH, Connelly A (2019) MRtrix3: a fast, flexible and open software framework for medical image processing and visualisation. Neuroimage 202:116137
doi: 10.1016/j.neuroimage.2019.116137
pubmed: 31473352
Choi JD, Moon Y, Kim HJ, Yim Y, Lee S, Moon WJ (2022) Choroid plexus volume and permeability at brain MRI within the Alzheimer disease clinical spectrum. Radiology 304:635–645
doi: 10.1148/radiol.212400
pubmed: 35579521
Ricigliano VAG, Stankoff B (2023) Choroid plexuses at the interface of peripheral immunity and tissue repair in multiple sclerosis. Curr Opin Neurol 36:214–221
doi: 10.1097/WCO.0000000000001160
pubmed: 37078651
Fleischer V, Gonzalez-Escamilla G, Ciolac D, Albrecht P, Kury P, Gruchot J, Dietrich M, Hecker C, Muntefering T, Bock S, Oshaghi M, Radetz A, Cerina M, Kramer J, Wachsmuth L, Faber C, Lassmann H, Ruck T, Meuth SG, Muthuraman M, Groppa S (2021) Translational value of choroid plexus imaging for tracking neuroinflammation in mice and humans. Proc Natl Acad Sci U S A 118
Jiang D, Liu L, Kong Y, Chen Z, Rosa-Neto P, Chen K, Ren L, Chu M, Wu L, Frontotemporal Lobar Degeneration Neuroimaging I (2023) Regional glymphatic abnormality in behavioral variant frontotemporal dementia. Ann Neurol
Mueller C, Fang YD, Jones C, McConathy JE, Raman F, Lapi SE, Younger JW (2023) Evidence of neuroinflammation in fibromyalgia syndrome: a [18F]DPA-714 positron emission tomography study. Pain
Johnson SE, McKnight CD, Lants SK, Juttukonda MR, Fusco M, Chitale R, Donahue PC, Claassen DO, Donahue MJ (2020) Choroid plexus perfusion and intracranial cerebrospinal fluid changes after angiogenesis. J Cereb Blood Flow Metab 40:1658–1671
doi: 10.1177/0271678X19872563
pubmed: 31500523
Holstein-Ronsbo S, Gan Y, Giannetto MJ, Rasmussen MK, Sigurdsson B, Beinlich FRM, Rose L, Untiet V, Hablitz LM, Kelley DH, Nedergaard M (2023) Glymphatic influx and clearance are accelerated by neurovascular coupling. Nat Neurosci 26:1042–1053
doi: 10.1038/s41593-023-01327-2
pubmed: 37264158
pmcid: 10500159
Chong PLH, Garic D, Shen MD, Lundgaard I, Schwichtenberg AJ (2022) Sleep, cerebrospinal fluid, and the glymphatic system: a systematic review. Sleep Med Rev 61:101572
doi: 10.1016/j.smrv.2021.101572
pubmed: 34902819
Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O’Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373–377
doi: 10.1126/science.1241224
pubmed: 24136970
Malcangio M (2019) Role of the immune system in neuropathic pain. Scand J Pain 20:33–37
doi: 10.1515/sjpain-2019-0138
pubmed: 31730538