Share:
Share this content in WeChat
X
Review
Research progress in MRI of anti-N-methyl-D-aspartate receptor encephalitis
LIU Hanjing  LUO Tianyou 

Cite this article as: Liu HJ, Luo TY. Research progress in MRI of anti-N-methyl-D-aspartate receptor encephalitis[J]. Chin J Magn Reson Imaging, 2022, 13(9): 139-143. DOI:10.12015/issn.1674-8034.2022.09.033.


[Abstract] Anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis is the most common type of autoimmune encephalitis, and its incidence is increasing year by year. There are many factors that can trigger the occurrence of anti-NMDAR encephalitis, which can be divided into neoplastic and non-neoplastic types. The clinical manifestations of anti-NMDAR encephalitis are complex and varied, and it is difficult to be diagnosed. Nearly half of the patients showed abnormal signals on conventional MRI for the first time, and advanced MRI is an effective supplement to deepen the understanding of imaging and pathology and pathophysiology of the disease. In this paper, the recent advances in conventional MRI and advanced MRI technology of anti-NMDAR encephalitis were reviewed, in order to improve the understanding of the disease.
[Keywords] anti-N-methyl-D-aspartate receptor encephalitis;encephalitis;magnetic resonance imaging

LIU Hanjing   LUO Tianyou*  

Department of Radiology, the First Affiliated Hospital of Chongqing Medical University, Chongqing 400016, China

*Luo TY, E-mail: ltychy@sina.com

Conflicts of interest   None.

Received  2022-05-06
Accepted  2022-09-07
DOI: 10.12015/issn.1674-8034.2022.09.033
Cite this article as: Liu HJ, Luo TY. Research progress in MRI of anti-N-methyl-D-aspartate receptor encephalitis[J]. Chin J Magn Reson Imaging, 2022, 13(9): 139-143.DOI:10.12015/issn.1674-8034.2022.09.033

[1]
Guan HZ, Wang JW. Consensus of Chinese experts on diagnosis and treatment of autoimmune encephalitis[J]. Chin J Neurol, 2017, 50(2): 91-98. DOI: 10.3760/cma.j.issn.1006-7876.2017.02.004.
[2]
Titulaer MJ, McCracken L, Gabilondo I, et al. Treatment and prognostic factors for long-term outcome in patients with anti-NMDA receptor encephalitis: an observational cohort study[J]. Lancet Neurol, 2013, 12(2): 157-165. DOI: 10.1016/s1474-4422(12)70310-1.
[3]
Florance NR, Davis RL, Lam C, et al. anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis in children and adolescents[J]. Ann Neurol, 2009, 66(1): 11-18. DOI: 10.1002/ana.21756.
[4]
Gable MS, Sheriff H, Dalmau J, et al. The frequency of autoimmune N-methyl-D-aspartate receptor encephalitis surpasses that of individual viral etiologies in young individuals enrolled in the California Encephalitis Project[J]. Clin Infect Dis, 2012, 54(7): 899-904. DOI: 10.1093/cid/cir1038.
[5]
Bost C, Chanson E, Picard G, et al. Malignant tumors in autoimmune encephalitis with anti-NMDA receptor antibodies[J]. J Neurol, 2018, 265(10): 2190-2200. DOI: 10.1007/s00415-018-8970-0.
[6]
Zrzavy T, Endmayr V, Bauer J, et al. Neuropathological variability within a spectrum of NMDAR-encephalitis[J]. Ann Neurol, 2021, 90(5): 725-737. DOI: 10.1002/ana.26223.
[7]
Yu Y, Liu J L, Tian DS. Anti-N-methyl-D-aspartate receptor encephalitis associated with chronic myelogenous leukemia, causality or coincidence? A case report[J/OL]. BMC Neurol, 2022, 22(1) [2022-05-05]. https://bmcneurol.biomedcentral.com/articles/10.1186/s12883-022-02675-5. DOI: 10.1186/s12883-022-02675-5.
[8]
Kobayashi Y, Sato M, Kinoshita M, et al. An elderly case of paraneoplastic anti-NMDA receptor encephalitis associated with small-cell lung cancer expressing NR1 subunits[J]. Intern Med, 2020, 59(18): 2307-2309. DOI: 10.2169/internalmedicine.4860-20.
[9]
Štourač P, Bednářová J, Zicháček P, et al. Autoimmune and limbic encephalitis: case series with some atypical variables in clinical practice[J]. Neurol Sci, 2022, 43(1): 687-690. DOI: 10.1007/s10072-021-05563-x.
[10]
Jiang H, Ye H, Wang Y, et al. Anti-N-methyl-D-aspartate receptor encephalitis associated with ovarian teratoma in south china-clinical features, treatment, immunopathology, and surgical outcomes of 21 cases[J/OL]. Dis Markers, 2021 [2022-08-30]. https://pubmed.ncbi.nlm.nih.gov/34093900. DOI: 10.1155/2021/9990382.
[11]
Hu S, Lan T, Bai R, et al. HSV encephalitis triggered anti-NMDAR encephalitis: a case report[J]. Neurol Sci, 2021, 42(3): 857-861. DOI: 10.1007/s10072-020-04785-9.
[12]
Cai X, Zhou H, Xie Y, et al. Anti-N-methyl-D-aspartate receptor encephalitis associated with acute Toxoplasma gondii infection: A case report[J/OL]. Medicine (Baltimore), 2018, 97(7) [2022-08-30]. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5839864/. DOI: 10.1097/md.0000000000009924.
[13]
Armangue T, Spatola M, Vlagea A, et al. Frequency, symptoms, risk factors, and outcomes of autoimmune encephalitis after herpes simplex encephalitis: a prospective observational study and retrospective analysis[J]. Lancet Neurol, 2018, 17(9): 760-772. DOI: 10.1016/s1474-4422(18)30244-8.
[14]
Gulec B, Kurucu H, Bozbay S, et al. Co-existence of multiple sclerosis and anti-NMDA receptor encephalitis: A case report and review of literature[J/OL]. Mult Scler Relat Disord, 2020, 42 [2022-08-30]. http://linkinghub.elsevierchealth.com/action/getSharedSiteSession?redirect=https%3A%2F%2Fmsard-journal.com%2Fretrieve%2Fpii%2FS2211034820301516&rc=0. DOI: 10.1016/j.msard.2020.102075.
[15]
Titulaer MJ, Höftberger R, Iizuka T, et al. Overlapping demyelinating syndromes and anti-N-methyl-D-aspartate receptor encephalitis[J]. Ann Neurol, 2014, 75(3): 411-428. DOI: 10.1002/ana.24117.
[16]
Panariello A, Bassetti R, Radice A, et al. Anti-NMDA receptor encephalitis in a psychiatric Covid-19 patient: A case report[J]. Brain Behav Immun, 2020, 87: 179-181. DOI: 10.1016/j.bbi.2020.05.054.
[17]
Burr T, Barton C, Doll E, et al. N-methyl-D-aspartate receptor encephalitis associated with COVID-19 infection in a toddler[J]. Pediatr Neurol, 2021, 114: 75-76. DOI: 10.1016/j.pediatrneurol.2020.10.002.
[18]
Dalmau J, Gleichman AJ, Hughes EG, et al. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies[J]. Lancet Neurol, 2008, 7(12): 1091-1098. DOI: 10.1016/s1474-4422(08)70224-2.
[19]
Dalmau J, Lancaster E, Martinez-Hernandez E, et al. Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis[J]. Lancet Neurol, 2011, 10(1): 63-74. DOI: 10.1016/s1474-4422(10)70253-2.
[20]
Viaccoz A, Desestret V, Ducray F, et al. Clinical specificities of adult male patients with NMDA receptor antibodies encephalitis[J]. Neurology, 2014, 82(7): 556-563. DOI: 10.1212/wnl.0000000000000126.
[21]
Yang RX, Gao FB. Advances in MRI studies on the influence of high altitude environmental exposure[J]. Int J Med Radiol, 2022, 45(4): 440-443, 448. DOI: 10.19300/j.2022.Z19683.
[22]
Zhang T, Duan Y, Ye J, et al. Brain MRI characteristics of patients with anti-N-methyl-D-aspartate receptor encephalitis and their associations with 2-year clinical outcome[J]. AJNR Am J Neuroradiol, 2018, 39(5): 824-829. DOI: 10.3174/ajnr.A5593.
[23]
Wang R, Lai X H, Liu X, et al. Brain magnetic resonance-imaging findings of anti-N-methyl-D-aspartate receptor encephalitis: a cohort follow-up study in Chinese patients[J]. J Neurol, 2018, 265(2): 362-369. DOI: 10.1007/s00415-017-8707-5.
[24]
Dou X, Li D, Wu F, et al. The clinical features, treatment and outcomes of 33 children from Northwestern China with anti-N-methyl-D-aspartate receptor encephalitis[J]. Neurol Res, 2022, 44(5): 429-438. DOI: 10.1080/01616412.2021.2000824.
[25]
Cheng BX, Zhou L, Yang C, et al. Clinical and MRI differential analysis of autoimmune encephalitis and viral encephalitis[J]. J Pract Radiol, 2019, 35(8): 1211-1216. DOI: 10.3969/j.issn.1002-1671.2019.08.003.
[26]
Elkhider H, Sharma R, Kapoor N, et al. Autoimmune encephalitis and seizures, cerebrospinal fluid, imaging, and EEG findings: a case series[J]. Neurol Sci, 2022, 43(4): 2669-2680. DOI: 10.1007/s10072-021-05617-0.
[27]
Xiang YY, Zeng C, Li YM. Imaging diagnosis and differential diagnosis of autoimmune encephalitis[J]. Chin J Radiol, 2020, 54(3): 256-260. DOI: 10.3760/cma.j.issn.1005-1201.2020.03.018.
[28]
Zhang W, Cui L, Wang W, et al. Early identification of anti–NMDA receptor encephalitis presenting cerebral lesions in unconventional locations on magnetic resonance imaging[J]. J Neuroimmunol, 2018, 320: 101-106. DOI: 10.1016/j.jneuroim.2018.03.015.
[29]
Neo S, Yeo T, Chen Z, et al. Acute radiological features facilitate diagnosis and prognosis of anti-N-methyl-D-aspartate receptor (NMDAR) and anti-voltage-gated potassium channel (VGKC) encephalitis in adults[J/OL]. J Neurol Sci, 2020, 419 [2022-8-30]. https://linkinghub.elsevier.com/retrieve/pii/S0022-510X(20)30552-9. DOI: 10.1016/j.jns.2020.117216.
[30]
Bian RJ, Xu YQ, Hu WZ, et al. Analysis of clinical and multimodal magnetic resonance imaging characteristics of autoimmune encephalitis[J]. Linchuang Yixue Yanjiu yu Shijian, 2020, 5(12): 14-17. DOI: 10.19347/j.cnki.2096-1413.202012006.
[31]
Song S, Tao Z, Shao LY, et al. Two cases of autoimmune encephalitis misdiagnosed as viral encephalitis[J]. Chin J Infect Dis, 2016, 34(7): 434-436. DOI: 10.3760/cma.j.issn.1000-6680.2016.07.013.
[32]
Lei C, Chang X, Li H, et al. Abnormal brain MRI findings in anti-N-methyl-D-aspartate receptor encephalitis and correlation with outcomes[J/OL]. Front Neurol, 2022, 13 [2022-08-30]. https://www.frontiersin.org/articles/10.3389/fneur.2022.834929/full. DOI: 10.3389/fneur.2022.834929.
[33]
Balu R, McCracken L, Lancaster E, et al. A score that predicts 1-year functional status in patients with anti-NMDA receptor encephalitis[J/OL]. Neurology, 2019, 92(3) [2022-08-30]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6340387/. DOI: 10.1212/wnl.0000000000006783.
[34]
Feng J, Yang M, Cui D, et al. Recurrence of anti-N-methyl-D-aspartate receptor encephalitis: a cohort study in central China[J/OL]. Front Neurol, 2022, 13 [2022-08-30]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8959942/. DOI: 10.3389/fneur.2022.832634.
[35]
Gomez-Figueroa E, Garcia-Estrada C, Paredes-Aragon E, et al. Brain MRI volumetric changes in the follow-up of patients with anti-NMDAR encephalitis[J/OL]. Clin Neurol Neurosurg, 2021, 209 [2022-08-30]. https://linkinghub.elsevier.com/retrieve/pii/S0303-8467(21)00437-6. DOI: 10.1016/j.clineuro.2021.106908.
[36]
Xu J, Guo Y, Li J, et al. Progressive cortical and sub-cortical alterations in patients with anti-N-methyl-D-aspartate receptor encephalitis[J]. J Neurol, 2022, 269(1): 389-398. DOI: 10.1007/s00415-021-10643-1.
[37]
Bartels F, Krohn S, Nikolaus M, et al. Clinical and magnetic resonance imaging outcome predictors in pediatric anti-N-methyl-D-aspartate receptor encephalitis[J]. Ann Neurol, 2020, 88(1): 148-159. DOI: 10.1002/ana.25754.
[38]
An YH, Qi ZG, Zhao ZL, et al. Characteristics of imaging findings on patients with anti-N-methyl-D-aspartate receptor encephalitis[J]. Zhongguo Quanke Yixue, 2019, 22(15): 1859-1863. DOI: 10.12114/j.issn.1007-9572.2018.00.400.
[39]
Phillips OR, Joshi SH, Narr KL, et al. Superficial white matter damage in anti-NMDA receptor encephalitis[J]. J Neurol Neurosurg Psychiatry, 2018, 89(5): 518-525. DOI: 10.1136/jnnp-2017-316822.
[40]
Liang Y, Cai L, Zhou X, et al. Voxel-based analysis and multivariate pattern analysis of diffusion tensor imaging study in anti-NMDA receptor encephalitis[J]. Neuroradiology, 2020, 62(2): 231-239. DOI: 10.1007/s00234-019-02321-x.
[41]
Shi D, Pan Z, Li X, et al. Diffusion coefficient orientation distribution function for diffusion magnetic resonance imaging[J/OL]. J Neurosci Methods, 2021, 348 [2022-08-30]. https://linkinghub.elsevier.com/retrieve/pii/S0165-0270(20)30409-X. DOI: 10.1016/j.jneumeth.2020.108986.
[42]
Qiao PG, Cheng X, Li G, et al. MR diffusional kurtosis imaging-based assessment of brain microstructural changes in patients with Moyamoya disease before and after revascularization[J]. AJNR Am J Neuroradiol, 2020, 41(2): 246-254. DOI: 10.3174/ajnr.A6392.
[43]
Li M, Chen X, Xu HL, et al. Brain structural abnormalities in the preclinical stage of Machado-Joseph disease/spinocerebellar ataxia type 3 (MJD/SCA3): evaluation by MRI morphometry, diffusion tensor imaging and neurite orientation dispersion and density imaging[J]. J Neurol, 2022, 269(6): 2989-2998. DOI: 10.1007/s00415-021-10890-2.
[44]
Miao A, Liu Q, Li Z, et al. Altered cerebral blood flow in patients with anti-NMDAR encephalitis[J]. J Neurol, 2020, 267(6): 1760-1773. DOI: 10.1007/s00415-020-09747-x.
[45]
Guo YY, Lu XY, Wu Y, et al. Correlation between cognitive impairment and cerebral perfusion changes in patients with N-methyl-D-aspartate receptor encephalitis[J]. Natl Med J China, 2020, 100(25): 1942-1946. DOI: 10.3760/cma.j.cn112137-20200108-00050.
[46]
Quality Management and Safety Management Group of Radiology Branch of Chinese Medical Association, Magnetic Resonance Group of Radiology Branch of Chinese Medical Association. Expert consensus on standardized application of arterial spin-labeled cerebral perfusion MRI[J]. Chin J Radiol, 2016, 50(11): 817-824. DOI: 10.3760/cma.j.issn.1005-1201.2016.11.003.
[47]
Wang K, Wu D, Ji C, et al. Abnormal brain activation during verbal memory encoding in postacute anti-N-methyl-D-aspartate receptor encephalitis[J/OL]. Brain Connect, 2021 [2022-08-30]. https://www.liebertpub.com/doi/10.1089/brain.2021.0046?url_ver=Z39.88-2003&rfr_id=ori%3Arid%3Acrossref.org&rfr_dat=cr_pub++0pubmed. DOI: 10.1089/brain.2021.0046.
[48]
Buckner RL, Andrews-Hanna JR, Schacter DL. The brain's default network: anatomy, function, and relevance to disease[J]. Ann N Y Acad Sci, 2008, 1124: 1-38. DOI: 10.1196/annals.1440.011.
[49]
Ogawa S, Lee TM, Kay AR, et al. Brain magnetic resonance imaging with contrast dependent on blood oxygenation[J]. Proc Natl Acad Sci USA, 1990, 87(24): 9868-9872. DOI: 10.1073/pnas.87.24.9868.
[50]
Zang Y, Jiang T, Lu Y, et al. Regional homogeneity approach to fMRI data analysis[J]. Neuroimage, 2004, 22(1): 394-400. DOI: 10.1016/j.neuroimage.2003.12.030.
[51]
Cai L, Liang Y, Huang H, et al. Cerebral functional activity and connectivity changes in anti-N-methyl-D-aspartate receptor encephalitis: A resting-state fMRI study[J/OL]. Neuroimage Clin, 2020, 25 [2022-08-30]. https://www.sciencedirect.com/science/article/pii/S2213158220300267?via%3Dihub. DOI: 10.1016/j.nicl.2020.102189.
[52]
Li C, Pang X, Shi K, et al. The insula is a hub for functional brain network in patients with anti-N-methyl-D-aspartate receptor encephalitis[J/OL]. Front Neurosci, 2021, 15 [2022-08-30]. https://www.frontiersin.org/articles/10.3389/fnins.2021.642390/full. DOI: 10.3389/fnins.2021.642390.
[53]
Wu P, Pang X, Liang X, et al. Correlation analysis between regional homogeneity and executive dysfunction in anti-N-methyl-D-aspartate receptor encephalitis patients[J]. Eur J Neurol, 2022, 29(1): 277-285. DOI: 10.1111/ene.15119.
[54]
Meer JNV, Breakspear M, Chang LJ, et al. Movie viewing elicits rich and reliable brain state dynamics[J/OL]. Nat Commun, 2020, 11(1) [2022-09-06]. https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/33020473/. DOI: 10.1038/s41467-020-18717-w.
[55]
Vidaurre D, Smith SM, Woolrich MW. Brain network dynamics are hierarchically organized in time. Proc Natl Acad Sci USA, 2017, 114(48): 12827-12832. DOI: 10.1073/pnas.1705120114.
[56]
Splendiani A, Felli V, Di Sibio A, et al. Magnetic resonance imaging and magnetic resonance spectroscopy in a young male patient with anti-N-methyl-D-aspartate receptor encephalitis and uncommon cerebellar involvement: A case report with review of the literature[J]. Neuroradiol J, 2016, 29(1): 30-35. DOI: 10.1177/1971400915609333.
[57]
Mariotto S, Tamburin S, Salviati A, et al. Anti-N-methyl-D-aspartate receptor encephalitis causing a prolonged depressive disorder evolving to inflammatory brain disease[J]. Case Rep Neurol, 2014, 6(1): 38-43. DOI: 10.1159/000358820.
[58]
Umamaheswara RV, Agrawal A, Murali KV, et al. The puzzle of choline and lipid peak on spectroscopy[J]. The Egyptian Journal of Radiology and Nuclear Medicine, 2014, 45(3): 903-907. DOI: 10.1016/j.ejrnm.2014.04.014.
[59]
Xiang Y, Dong X, Zeng C, et al. Clinical variables, deep learning and radiomics features help predict the prognosis of adult anti-N-methyl-D-aspartate receptor encephalitis early: a two-center study in southwest China[J/OL]. Front Immunol, 2022, 13 [2022-08-30]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9199424/. DOI: 10.3389/fimmu.2022.913703.
[60]
Wang J, Duan Y, Zhang T, et al. Aberrant multimodal brain networks in patients with anti-NMDA receptor encephalitis[J]. CNS Neurosci Ther, 2021, 27(6): 652-663. DOI: 10.1111/cns.13632.

PREV Research progress of T2-FLAIR mismatch sign in predicting molecular typing of lower-grade glioma
NEXT Progress in the clinical application of compressed sensing technology in brain MRI
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn