Neuroimaging characteristics may aid in diagnosis, subtyping, and prognosis in autoimmune encephalitis.
Atrophy
Autoimmune encephalitis
MRI
PET
Prognosis
Journal
Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175
Informations de publication
Date de publication:
Apr 2023
Apr 2023
Historique:
received:
30
07
2022
accepted:
19
11
2022
pubmed:
10
12
2022
medline:
22
3
2023
entrez:
9
12
2022
Statut:
ppublish
Résumé
To examine the utility of neuroimaging characteristics as biomarkers of prognosis in seropositive autoimmune encephalitis (AE). In this multi-center study, we retrospectively analyzed 66 cases of seropositive AE. The MRI and PET imaging was assessed by independent visual inspection. Whole brain and regional volumes were imputed by IcoMetrix, an automated volumetric assessment package. The modified Rankin Scale (mRS) was utilized to assess the patients' follow-up disability. Other outcomes were mortality, first line treatment failure, medial temporal lobe (MTL) atrophy, and clinical relapse. Univariate and multivariable regression analysis was performed. Abnormalities on MRI were detected in 35.1% of patients, while PET was abnormal in 46.4%. Initial median whole brain and hippocampal volumes were below the 5th and 20th percentile respectively compared to an age-matched healthy database. After a median follow-up of 715 days, 85.2% had good functional outcome (mRS ≤ 2). Nine patients developed MTL atrophy during follow-up. On multivariable analysis, inflammatory MTL changes were associated with development of MTL atrophy (HR 19.6, p = 0.007) and initial hippocampal volume had an inverse relationship with mortality (HR 0.04, p = 0.011). Patients who developed MTL atrophy had a reduced chance of good final mRS (HR 0.16, p = 0.015). Neuroimaging on initial hospital admission may be provide important diagnostic and prognostic information. This study demonstrates that structural and inflammatory changes of the MTL may have importance in clinical and radiological prognosis in seropositive AE.
Identifiants
pubmed: 36481972
doi: 10.1007/s10072-022-06523-9
pii: 10.1007/s10072-022-06523-9
doi:
Types de publication
Multicenter Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1327-1340Subventions
Organisme : National Health and Medical Research Council
ID : APP 1201062
Investigateurs
Sarah Griffiths
(S)
Tiffany Rushen
(T)
Tracie Tan
(T)
Charles Malpas
(C)
Amy Halliday
(A)
Rubina Alpitsis
(R)
Nabil Seery
(N)
David Tarlinton
(D)
Steve Reddel
(S)
Todd Hardy
(T)
Bruce Taylor
(B)
Brian Long
(B)
Tissa Wijeratne
(T)
Owen White
(O)
Jo Fielding
(J)
Meng Tan
(M)
Jayashri Kulkarni
(J)
Robert Bourke
(R)
Dennis Velakoulis
(D)
Ernie Butler
(E)
Catherine Meade
(C)
Stefan Blum
(S)
Sudarshini Ramanathan
(S)
Geneieve Skinner
(G)
Miri Forcadela
(M)
Simon Broadley
(S)
Yang Tran
(Y)
Andrew Swayne
(A)
Meaghan Clough
(M)
Informations de copyright
© 2022. Fondazione Società Italiana di Neurologia.
Références
Heine J, Pruss H, Bartsch T, Ploner CJ, Paul F, Finke C (2015) Imaging of autoimmune encephalitis–relevance for clinical practice and hippocampal function. Neuroscience 309:68–83
pubmed: 26012492
doi: 10.1016/j.neuroscience.2015.05.037
Graus F, Titulaer MJ, Balu R, Benseler S, Bien CG, Cellucci T, Cortese I, Dale RC, Gelfand JM, Geschwind M, Glaser CA, Honnorat J, Hoftberger R, Iizuka T, Irani SR, Lancaster E, Leypoldt F, Pruss H, Rae-Grant A, Reindl M, Rosenfeld MR, Rostasy K, Saiz A, Venkatesan A, Vincent A, Wandinger KP, Waters P, Dalmau J (2016) A clinical approach to diagnosis of autoimmune encephalitis. Lancet Neurol 15:391–404
pubmed: 26906964
pmcid: 5066574
doi: 10.1016/S1474-4422(15)00401-9
Kramer RE, Luders H, Lesser RP, Weinstein MR, Dinner DS, Morris HH, Wyllie E (1987) Transient focal abnormalities of neuroimaging studies during focal status epilepticus. Epilepsia 28:528–532
pubmed: 3653056
doi: 10.1111/j.1528-1157.1987.tb03683.x
Xiang T, Li G, Liang Y, Zhou J (2014) A wide spectrum of variably periictal MRI abnormalities induced by a single or a cluster of seizures. J Neurol Sci 343:167–172
pubmed: 24950900
doi: 10.1016/j.jns.2014.06.001
Williams J, Mullins G, Delanty N, Bede P, Doherty CP (2017) The spectrum of peri-ictal MRI changes; four illustrative cases. Seizure 50:189–193
pubmed: 28709144
doi: 10.1016/j.seizure.2017.06.024
Kamble N, Netravathi M, Saini J, Mahadevan A, Yadav R, Nalini A, Pal PK, Satishchandra P (2015) Clinical and imaging characteristics of 16 patients with autoimmune neuronal synaptic encephalitis. Neurol India 63:687–696
pubmed: 26448226
doi: 10.4103/0028-3886.166532
Baumgartner A, Rauer S, Mader I, Meyer PT (2013) Cerebral FDG-PET and MRI findings in autoimmune limbic encephalitis: correlation with autoantibody types. J Neurol 260:2744–2753
pubmed: 23900756
doi: 10.1007/s00415-013-7048-2
Finke C, Kopp UA, Pajkert A, Behrens JR, Leypoldt F, Wuerfel JT, Ploner CJ, Pruss H, Paul F (2016) Structural hippocampal damage following anti-N-methyl-D-aspartate receptor encephalitis. Biol Psychiatry 79:727–734
pubmed: 25866294
doi: 10.1016/j.biopsych.2015.02.024
Finke C, Pruss H, Heine J, Reuter S, Kopp UA, Wegner F, Then Bergh F, Koch S, Jansen O, Munte T, Deuschl G, Ruprecht K, Stocker W, Wandinger KP, Paul F, Bartsch T (2017) Bartsch, Evaluation of cognitive deficits and structural hippocampal damage in encephalitis with leucine-rich, glioma-inactivated 1 antibodies. JAMA Neurol 74:50–59
pubmed: 27893017
doi: 10.1001/jamaneurol.2016.4226
Urbach H, Soeder BM, Jeub M, Klockgether T, Meyer B, Bien CG (2006) Serial MRI of limbic encephalitis. Neuroradiology 48:380–386
pubmed: 16586118
doi: 10.1007/s00234-006-0069-0
Kotsenas AL, Watson RE, Pittock SJ, Britton JW, Hoye SL, Quek AM, Shin C, Klein CJ (2014) MRI findings in autoimmune voltage-gated potassium channel complex encephalitis with seizures: one potential etiology for mesial temporal sclerosis. AJNR Am J Neuroradiol 35:84–89
pubmed: 23868165
pmcid: 7966496
doi: 10.3174/ajnr.A3633
Wei YC, Liu CH, Lin JJ, Lin KJ, Huang KL, Lee TH, Chang YJ, Peng TI, Lin KL, Chang TY, Chang CH, Kuo HC, Chang KH, Cheng MY, Huang CC (2013) Rapid progression and brain atrophy in anti-AMPA receptor encephalitis. J Neuroimmunol 261:129–133
pubmed: 23796872
doi: 10.1016/j.jneuroim.2013.05.011
Iizuka T, Kaneko J, Tominaga N, Someko H, Nakamura M, Ishima D, Kitamura E, Masuda R, Oguni E, Yanagisawa T, Kanazawa N, Dalmau J, Nishiyama K (2016) Association of progressive cerebellar atrophy with long-term outcome in patients with anti-N-methyl-d-aspartate receptor encephalitis. JAMA Neurol 73:706–713
pubmed: 27111481
doi: 10.1001/jamaneurol.2016.0232
Arbizu J, Giuliani A, Gallego Perez-Larraya J, Riverol M, Jonsson C, Garcia-Garcia B, Morales M, Imaz L, Pagani M (2017) Emerging clinical issues and multivariate analyses in PET investigations. Q J Nucl Med Mol Imaging 61:386–404
pubmed: 28750498
doi: 10.23736/S1824-4785.17.03024-2
Solnes LB, Jones KM, Rowe SP, Pattanayak P, Nalluri A, Venkatesan A, Probasco JC, Javadi MS (2017) Diagnostic value of (18)F-FDG PET/CT versus MRI in the setting of antibody-specific autoimmune encephalitis. J Nucl Med 58:1307–1313
pubmed: 28209905
pmcid: 6944181
doi: 10.2967/jnumed.116.184333
Lv RJ, Pan J, Zhou G, Wang Q, Shao XQ, Zhao XB, Liu J (2019) Semi-quantitative FDG-PET analysis increases the sensitivity compared with visual analysis in the diagnosis of autoimmune encephalitis. Front Neurol 10:576
pubmed: 31244751
pmcid: 6563773
doi: 10.3389/fneur.2019.00576
Probasco JC, Solnes L, Nalluri A, Cohen J, Jones KM, Zan E, Javadi MS, Venkatesan A (2017) Abnormal brain metabolism on FDG-PET/CT is a common early finding in autoimmune encephalitis. Neurol Neuroimmunol NeuroInflammation 4:e352
doi: 10.1212/NXI.0000000000000352
Probasco JC, Solnes L, Nalluri A, Cohen J, Jones KM, Zan E, Javadi MS, Venkatesan A (2018) Decreased occipital lobe metabolism by FDG-PET/CT: an anti-NMDA receptor encephalitis biomarker. Neurol Neuroimmunol Neuroinflammation 5:e413
doi: 10.1212/NXI.0000000000000413
Harris PA, Taylor R, Minor BL, Elliott V, Fernandez M, O’Neal L, McLeod L, Delacqua G, Delacqua F, Kirby J, Duda SN, Consortium RE (2019) The REDCap consortium: building an international community of software platform partners. J Biomed Inform 95:103208
pubmed: 31078660
pmcid: 7254481
doi: 10.1016/j.jbi.2019.103208
Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG (2009) Research electronic data capture (REDCap)–a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 42:377–381
pubmed: 18929686
doi: 10.1016/j.jbi.2008.08.010
Titulaer MJ, McCracken L, Gabilondo I, Armangue T, Glaser C, Iizuka T, Honig LS, Benseler SM, Kawachi I, Martinez-Hernandez E, Aguilar E, Gresa-Arribas N, Ryan-Florance N, Torrents A, Saiz A, Rosenfeld MR, Balice-Gordon R, Graus F, Dalmau J (2013) Treatment and prognostic factors for long-term outcome in patients with anti-NMDA receptor encephalitis: an observational cohort study. Lancet Neurol 12:157–165
pubmed: 23290630
pmcid: 3563251
doi: 10.1016/S1474-4422(12)70310-1
Cendes F, Theodore WH, Brinkmann BH, Sulc V, Cascino GD (2016) Neuroimaging of epilepsy. Handb Clin Neurol 136:985–1014
pubmed: 27430454
pmcid: 5256664
doi: 10.1016/B978-0-444-53486-6.00051-X
Finkelsztejn A, Fragoso YD, Bastos EA, Duarte JA, Varela JS, Houbrechts R, Sima D, Van Hecke W (2018) Intercontinental validation of brain volume measurements using MSmetrix. Neuroradiol J 31:147–149
pubmed: 28730868
doi: 10.1177/1971400917721521
Fragoso YD, Wille PR, Abreu M, Brooks JBB, Dias RM, Duarte JA, Farage L, Finkelsztejn A, Frohlich AC, Goncalves MVM, Guedes BVS, Medeiros L, Oliveira RA, Ribas FD, da Rocha FCG, Santos GAC, Scorcine C, da Silveira GL, Spedo CT, Tauil CB, Varela JS, Vieira VLF, Brazilian Brain Volume Studies (2017) Brazilian Brain Volume Studies, Correlation of clinical findings and brain volume data in multiple sclerosis. J Clin Neurosci 44:155–157
pubmed: 28676309
doi: 10.1016/j.jocn.2017.06.006
Storelli L, Rocca MA, Pagani E, Van Hecke W, Horsfield MA, De Stefano N, Rovira A, Sastre-Garriga J, Palace J, Sima D, Smeets D, Filippi M, MS Group (2018) Measurement of whole-brain and gray matter atrophy in multiple sclerosis: assessment with MR imaging. Radiology 288:554–564
pubmed: 29714673
doi: 10.1148/radiol.2018172468
Steenwijk MD, Amiri H, Schoonheim MM, de Sitter A, Barkhof F, Pouwels PJW, Vrenken H (2017) Agreement of MSmetrix with established methods for measuring cross-sectional and longitudinal brain atrophy. Neuroimage Clin 15:843–853
pubmed: 28794970
pmcid: 5540882
doi: 10.1016/j.nicl.2017.06.034
Wang C, Beadnall HN, Hatton SN, Bader G, Tomic D, Silva DG, Barnett MH (2016) Automated brain volumetrics in multiple sclerosis: a step closer to clinical application. J Neurol Neurosurg Psychiatry 87:754–757
pubmed: 27071647
doi: 10.1136/jnnp-2015-312304
Minoshima S, Frey KA, Koeppe RA, Foster NL, Kuhl DE (1995) A diagnostic approach in Alzheimer’s disease using three-dimensional stereotactic surface projections of fluorine-18-FDG PET. J Nucl Med 36:1238–1248
pubmed: 7790950
van Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J (1988) Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19:604–607
pubmed: 3363593
doi: 10.1161/01.STR.19.5.604
Lee WJ, Lee ST, Byun JI, Sunwoo JS, Kim TJ, Lim JA, Moon J, Lee HS, Shin YW, Lee KJ, Kim S, Jung KH, Jung KY, Chu K, Lee SK (2016) Rituximab treatment for autoimmune limbic encephalitis in an institutional cohort. Neurology 86:1683–1691
pubmed: 27037228
doi: 10.1212/WNL.0000000000002635
Lee WJ, Lee ST, Moon J, Sunwoo JS, Byun JI, Lim JA, Kim TJ, Shin YW, Lee KJ, Jun JS, Lee HS, Kim S, Park KI, Jung KH, Jung KY, Kim M, Lee SK, Chu K (2016) Tocilizumab in autoimmune encephalitis refractory to rituximab: an institutional cohort study. Neurotherapeutics 13:824–832
pubmed: 27215218
pmcid: 5081109
doi: 10.1007/s13311-016-0442-6
de Montmollin E, Demeret S, Brule N, Conrad M, Dailler F, Lerolle N, Navellou JC, Schwebel C, Alves M, Cour M, Engrand N, Tonnelier JM, Maury E, Ruckly S, Picard G, Rogemond V, Magalhaes E, Sharshar T, Timsit JF, Honnorat J, Sonneville R, ENCEPHALITICA Study Group (2017) Anti-N-methyl-d-aspartate receptor encephalitis in adult patients requiring intensive care. Am J Respir Crit Care Med 195:491–499
pubmed: 27552490
doi: 10.1164/rccm.201603-0507OC
Titulaer MJ, McCracken L, Gabilondo I, Iizuka T, Kawachi I, Bataller L, Torrents A, Rosenfeld MR, Balice-Gordon R, Graus F, Dalmau J (2013) Late-onset anti-NMDA receptor encephalitis. Neurology 81:1058–1063
pubmed: 23946310
pmcid: 3795591
doi: 10.1212/WNL.0b013e3182a4a49c
Balu R, McCracken L, Lancaster E, Graus F, Dalmau J, Titulaer MJ (2019) A score that predicts 1-year functional status in patients with anti-NMDA receptor encephalitis. Neurology 92:e244–e252
pubmed: 30578370
pmcid: 6340387
doi: 10.1212/WNL.0000000000006783
Arino H, Armangue T, Petit-Pedrol M, Sabater L, Martinez-Hernandez E, Hara M, Lancaster E, Saiz A, Dalmau J, Graus F (2016) Anti-LGI1-associated cognitive impairment: presentation and long-term outcome. Neurology 87:759–765
pubmed: 27466467
pmcid: 4999321
doi: 10.1212/WNL.0000000000003009
Flanagan EP, Kotsenas AL, Britton JW, McKeon A, Watson RE, Klein CJ, Boeve BF, Lowe V, Ahlskog JE, Shin C, Boes CJ, Crum BA, Laughlin RS, Pittock SJ (2015) Basal ganglia T1 hyperintensity in LGI1-autoantibody faciobrachial dystonic seizures. Neurol Neuroimmunol Neuroinflammation 2:e161
doi: 10.1212/NXI.0000000000000161
Malter MP, Frisch C, Schoene-Bake JC, Helmstaedter C, Wandinger KP, Stoecker W, Urbach H, Surges R, Elger CE, Vincent AV, Bien CG (2014) Outcome of limbic encephalitis with VGKC-complex antibodies: relation to antigenic specificity. J Neurol 261:1695–1705
pubmed: 24935858
doi: 10.1007/s00415-014-7408-6
Lang B, Makuch M, Moloney T, Dettmann I, Mindorf S, Probst C, Stoecker W, Buckley C, Newton CR, Leite MI, Maddison P, Komorowski L, Adcock J, Vincent A, Waters P, Irani SR (2017) Intracellular and non-neuronal targets of voltage-gated potassium channel complex antibodies. J Neurol Neurosurg Psychiatry 88:353–361
pubmed: 28115470
doi: 10.1136/jnnp-2016-314758
Shao X, Fan S, Luo H, Wong TY, Zhang W, Guan H, Qiu A (2020) Brain magnetic resonance imaging characteristics of anti-leucine-rich glioma-inactivated 1 encephalitis and their clinical relevance: a single-center study in China. Front Neurol 11:618109
pubmed: 33510707
doi: 10.3389/fneur.2020.618109
Laurikainen H, Isotupa I, Nyman M, Ilonen T, Nummelin T, Salokangas RKR, Hietala J (2019) Longitudinal brain morphology in anti-NMDA receptor encephalitis: a case report with controls. BMC Psychiatry 19:145
pubmed: 31077184
pmcid: 6511133
doi: 10.1186/s12888-019-2141-4
Gomez-Figueroa E, Garcia-Estrada C, Paredes-Aragon E, Salado-Burbano J, Cortes-Enriquez F, Marrufo-Melendez O, Espinola-Nadurille M, Ramirez-Bermudez J, Rivas-Alonso V, Corona T, Flores-Rivera J (2021) Brain MRI volumetric changes in the follow-up of patients with anti-NMDAr encephalitis. Clin Neurol Neurosurg 209:106908
pubmed: 34488009
doi: 10.1016/j.clineuro.2021.106908
Bartels F, Krohn S, Nikolaus M, Johannsen J, Wickstrom R, Schimmel M, Hausler M, Berger A, Breu M, Blankenburg M, Stoffels J, Hendricks O, Bernert G, Kurlemann G, Knierim E, Kaindl A, Rostasy K, Finke C (2020) Clinical and magnetic resonance imaging outcome predictors in pediatric anti-N-methyl-D-aspartate receptor encephalitis. Ann Neurol 88:148–159
pubmed: 32314416
doi: 10.1002/ana.25754
Dieleman N, Koek HL, Hendrikse J (2017) Short-term mechanisms influencing volumetric brain dynamics. Neuroimage Clin 16:507–513
pubmed: 28971004
pmcid: 5609861
doi: 10.1016/j.nicl.2017.09.002
Iizuka T, Yoshii S, Kan S, Hamada J, Dalmau J, Sakai F, Mochizuki H (2010) Reversible brain atrophy in anti-NMDA receptor encephalitis: a long-term observational study. J Neurol 257:1686–1691
pubmed: 20517615
pmcid: 3071951
doi: 10.1007/s00415-010-5604-6
Nillo RM, Broce IJ, Uzgil B, Singhal NS, Glastonbury CM, Hess CP, Barkovich JA, Desikan RS, Sugrue LP (2021) Longitudinal analysis of regional brain changes in anti-NMDAR encephalitis: a case report. BMC Neurol 21:412
pubmed: 34706674
pmcid: 8554978
doi: 10.1186/s12883-021-02446-8
Ge J, Deng B, Guan Y, Bao W, Wu P, Chen X, Zuo C (2021) Distinct cerebral (18)F-FDG PET metabolic patterns in anti-N-methyl-D-aspartate receptor encephalitis patients with different trigger factors. Ther Adv Neurol Disord 14:1756286421995635
pubmed: 33717212
pmcid: 7919218
doi: 10.1177/1756286421995635
Fragoso YD, Willie PR, Goncalves MVM, Brooks JBB (2017) Critical analysis on the present methods for brain volume measurements in multiple sclerosis. Arq Neuropsiquiatr 75:464–469
pubmed: 28746434
doi: 10.1590/0004-282x20170072
Gonzalez-Villa S, Valverde S, Cabezas M, Pareto D, Vilanova JC, Ramio-Torrenta L, Rovira A, Oliver A, Llado X (2017) Evaluating the effect of multiple sclerosis lesions on automatic brain structure segmentation. Neuroimage Clin 15:228–238
pubmed: 28540179
pmcid: 5430150
doi: 10.1016/j.nicl.2017.05.003
Broadley J, Seneviratne U, Beech P, Buzzard K, Butzkueven H, O’Brien T, Monif M (2019) Prognosticating autoimmune encephalitis: a systematic review. J Autoimmun 96:24–34
pubmed: 30595145
doi: 10.1016/j.jaut.2018.10.014