Radiopraxis 2023; 16(02): E54-E73
DOI: 10.1055/a-2058-1958
CPD-Fortbildung

FDG-PET-Bildgebung der limbischen Enzephalitis

FDG-PET imaging of limbic encephalitis
Ralph Buchert
,
Sebastian Rauer
,
Philipp T. Meyer

Bei der limbischen Enzephalitis liefert die zerebrale FDG-PET essenzielle Informationen zur Unterstützung von Diagnose, Prognose und Therapiekontrolle. Mit zunehmender Bedeutung der limbischen Enzephalitis als „not to miss“-Diagnose wird der Stellenwert der zerebralen FDG-PET bei dieser Fragestellung weiter steigen. Zudem kommt der FDG-PET-Ganzkörperaufnahme bei Verdacht auf eine paraneoplastische Genese und unauffälligem Tumorscreening in den Routineuntersuchungen eine Schlüsselrolle zu.



Publikationsverlauf

Artikel online veröffentlicht:
02. Juni 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • Literatur

  • 1 Dubey D, Pittock SJ, Kelly CR. et al. Autoimmune encephalitis epidemiology and a comparison to infectious encephalitis. Ann Neurol 2018; 83: 166-177
  • 2 Uy CE, Binks S, Irani SR.. Autoimmune encephalitis: clinical spectrum and management. Pract Neurol 2021; 21: 412-423
  • 3 [Anonym]. Fortschritte bei der Autoimmunenzephalitis: spezifische Diagnose, sequenzielle Therapie und Netflix. In: Deutsche Gesellschaft für Neurologie; 2018
  • 4 Kelley BP, Patel SC, Marin HL. et al. Autoimmune Encephalitis: Pathophysiology and Imaging Review of an Overlooked Diagnosis. Am J Neuroradiol 2017; 38: 1070-1078
  • 5 Abboud H, Probasco JC, Irani S. et al. Autoimmune encephalitis: proposed best practice recommendations for diagnosis and acute management. J Neurol Neurosurg Psychiatry 2021; 92: 757-768
  • 6 Baumgartner A, Rauer S, Hottenrott T. et al. Admission diagnoses of patients later diagnosed with autoimmune encephalitis. J Neurol 2019; 266: 124-132
  • 7 Doss S, Wandinger KP, Hyman BT. et al. High prevalence of NMDA receptor IgA/IgM antibodies in different dementia types. Ann Clin Transl Neurol 2014; 1: 822-832
  • 8 Corsellis JA, Goldberg GJ, Norton AR.. „Limbic encephalitis“ and its association with carcinoma. Brain 1968; 91: 481-496
  • 9 Haberlandt E, Bast T, Ebner A. et al. Limbic encephalitis in children and adolescents. Arch Dis Child 2011; 96: 186-191
  • 10 Gultekin SH, Rosenfeld MR, Voltz R. et al. Paraneoplastic limbic encephalitis: neurological symptoms, immunological findings and tumour association in 50 patients. Brain 2000; 123: 1481-1494
  • 11 Bien CG, Schulze-Bonhage A, Deckert M. et al. Limbic encephalitis not associated with neoplasm as a cause of temporal lobe epilepsy. Neurology 2000; 55: 1823-1828
  • 12 Graus F, Escudero D, Oleaga L. et al. Syndrome and outcome of antibody-negative limbic encephalitis. Eur J Neurol 2018; 25: 1011-1016
  • 13 van Sonderen A, Thijs RD, Coenders EC. et al. Anti-LGI1 encephalitis: Clinical syndrome and long-term follow-up. Neurology 2016; 87: 1449-1456
  • 14 Bien CG.. Principles of autoimmune and paraneoplastic encephalitis. Nervenarzt 2018; 89: 934-941
  • 15 Dalmau J, Graus F.. Antibody-Mediated Encephalitis. N Engl J Med 2018; 378: 840-851
  • 16 Graus F, Titulaer MJ, Balu R. et al. A clinical approach to diagnosis of autoimmune encephalitis. Lancet Neurol 2016; 15: 391-404
  • 17 Hellwig S, Domschke K, Meyer PT.. Update on PET in neurodegenerative and neuroinflammatory disorders manifesting on a behavioural level: imaging for differential diagnosis. Curr Opin Neurol 2019; 32: 548-556
  • 18 Albert ML, Darnell JC, Bender A. et al. Tumor-specific killer cells in paraneoplastic cerebellar degeneration. Nat Med 1998; 4: 1321-1324
  • 19 Bien CG, Vincent A, Barnett MH. et al. Immunopathology of autoantibody-associated encephalitides: clues for pathogenesis. Brain 2012; 135: 1622-1638
  • 20 Cellucci T, Van Mater H, Graus F. et al. Clinical approach to the diagnosis of autoimmune encephalitis in the pediatric patient. Neurol Neuroimmunol Neuroinflamm 2020; 7
  • 21 Sun B, Ramberger M, O'Connor KC. et al. The B cell immunobiology that underlies CNS autoantibody-mediated diseases. Nat Rev Neurol 2020; 16: 481-492
  • 22 Troscher AR, Klang A, French M. et al. Selective Limbic Blood-Brain Barrier Breakdown in a Feline Model of Limbic Encephalitis with LGI1 Antibodies. Front Immunol 2017; 8: 1364
  • 23 van Sonderen A, Petit-Pedrol M, Dalmau J. et al. The value of LGI1, Caspr2 and voltage-gated potassium channel antibodies in encephalitis. Nat Rev Neurol 2017; 13: 290-301
  • 24 Kornau HC, Kreye J, Stumpf A. et al. Human Cerebrospinal fluid monoclonal LGI1 autoantibodies increase neuronal excitability. Ann Neurol 2020; 87: 405-418
  • 25 Velasco R, Villagran M, Jove M. et al. Encephalitis Induced by Immune Checkpoint Inhibitors: A Systematic Review. JAMA Neurol 2021; 78: 864-873
  • 26 Binks S, Varley J, Lee W. et al. Distinct HLA associations of LGI1 and CASPR2-antibody diseases. Brain 2018; 141: 2263-2271
  • 27 Dalmau J, Geis C, Graus F.. Autoantibodies to Synaptic Receptors and Neuronal Cell Surface Proteins in Autoimmune Diseases of the Central Nervous System. Physiol Rev 2017; 97: 839-887
  • 28 Shir D, Day GS.. Deciphering the contributions of neuroinflammation to neurodegeneration: lessons from antibodymediated encephalitis and coronavirus disease 2019. Curr Opin Neurol 2022; 35: 212-219
  • 29 Kunchok A, McKeon A, Zekeridou A. et al. Autoimmune/Paraneoplastic Encephalitis Antibody Biomarkers: Frequency, Age, and Sex Associations. Mayo Clin Proc 2022; 97: 547-559
  • 30 Budhram A, Leung A, Nicolle MW. et al. Diagnosing autoimmune limbic encephalitis. Can Med Assoc J 2019; 191: E529-E534
  • 31 Kao YC, Lin MI, Weng WC. et al. Neuropsychiatric Disorders Due to Limbic Encephalitis: Immunologic Aspect. Int J Mol Sci 2020; 22
  • 32 Prüß H.. Neuroimmunologie: Neues zur limbischen Enzephalitis. Akt Neurol 2013; 40: 127-136
  • 33 Younger DS.. Autoimmune Encephalitides. Neurol Clin 2019; 37: 359-381
  • 34 Behrman S, Lennox B.. Autoimmune encephalitis in the elderly: who to test and what to test for. Evid Based Ment Health 2019; 22: 172-176
  • 35 Sechi E, Flanagan EP.. Diagnosis and Management of Autoimmune Dementia. Curr Treat Options Neurol 2019; 21: 11
  • 36 Darnell RB, Posner JB.. A new cause of limbic encephalopathy. Brain 2005; 128: 1745-1746
  • 37 Najjar S, Pearlman D, Zagzag D. et al. Spontaneously resolving seronegative autoimmune limbic encephalitis. Cogn Behav Neurol 2011; 24: 99-105
  • 38 Neurologie DGf. Immunvermittelte Erkrankungen der grauen ZNS-Substanz sowie Neurosarkoidose. AWMF-Registernummer 030/120; 2012
  • 39 Neurologie DGf. Paraneoplastische neurologische Syndrome (S1-Leitlinine mit interdisziplinärer Abstimmung). AWMF-Registernummer 030/064; 2015
  • 40 Rossling R, Pruss H.. Apheresis in Autoimmune Encephalitis and Autoimmune Dementia. J Clin Med 2020; 9
  • 41 Finke C, Pruss H, Heine J. et al. Evaluation of Cognitive Deficits and Structural Hippocampal Damage in Encephalitis With Leucine-Rich, Glioma-Inactivated 1 Antibodies. JAMA Neurol 2017; 74: 50-59
  • 42 Thompson J, Bi M, Murchison AG. et al. The importance of early immunotherapy in patients with faciobrachial dystonic seizures. Brain 2018; 141: 348-356
  • 43 Vollmer TL, McCarthy M.. Autoimmune encephalitis A more treatable tragedy if diagnosed early. Neurology 2016; 86: 1655-1656
  • 44 Vincent A, Buckley C, Schott JM. et al. Potassium channel antibody-associated encephalopathy: a potentially immunotherapy-responsive form of limbic encephalitis. Brain 2004; 127: 701-712
  • 45 Abboud H, Probasco J, Irani SR. et al. Autoimmune encephalitis: proposed recommendations for symptomatic and long-term management. J Neurol Neurosurg Psychiatry 2021;
  • 46 Kohler J, Hufschmidt A, Hermle L. et al. Limbic Encephalitis -2 Cases. J Neuroimmunol 1988; 20: 177-178
  • 47 Liu X, Yu T, Zhao X. et al. 18) F-fluorodeoxy-glucose positron emission tomography pattern and prognostic predictors in patients with anti-GABAB receptor encephalitis. CNS Neurosci Ther 2022; 28: 269-278
  • 48 Dinoto A, Cheli M, Ajcevic M. et al. ASL MRI and 18F-FDG-PET in autoimmune limbic encephalitis: clues from two paradigmatic cases. Neurol Sci 2021; 42: 3423-3425
  • 49 Sarria-Estrada S, Toledo M, Lorenzo-Bosquet C. et al. Neuroimaging in status epilepticus secondary to paraneoplastic autoimmune encephalitis. Clin Radiol 2014; 69: 795-803
  • 50 Mutke MA, Madai VI, von Samson-Himmelstjerna FC. et al. Clinical evaluation of an arterial-spin-labeling product sequence in steno-occlusive disease of the brain. PLoS One 2014; 9: e87143
  • 51 Heine J, Pruss H, Bartsch T. et al. Imaging of autoimmune encephalitis-Relevance for clinical practice and hippocampal function. Neuroscience 2015; 309: 68-83
  • 52 Ball C, Fisicaro R, Morris L. et al. Brain on fire: an imagingbased review of autoimmune encephalitis. Clin Imaging 2022; 84: 1-30
  • 53 Blanc F, Ruppert E, Kleitz C. et al. Acute limbic encephalitis and glutamic acid decarboxylase antibodies: a reality. J Neurol Sci 2009; 287: 69-71
  • 54 Troester F, Weske G, Schlaudraff E. et al. Image of the month. FDG-PET in paraneoplastic limbic encephalitis. Eur J Nucl Med Mol Imaging 2009; 36: 539
  • 55 Kassubek J, Juengling FD, Nitzsche EU. et al. Limbic encephalitis investigated by 18FDG-PET and 3D MRI. J Neuroimaging 2001; 11: 55-59
  • 56 Provenzale JM, Barboriak DP, Coleman RE.. Limbic encephalitis: comparison of FDG PET and MR imaging findings. AJR Am J Roentgenol 1998; 170: 1659-1660
  • 57 Malter MP, Helmstaedter C, Urbach H. et al. Antibodies to glutamic acid decarboxylase define a form of limbic encephalitis. Ann Neurol 2010; 67: 470-478
  • 58 Spatola M, Stojanova V, Prior JO. et al. Serial brain (1)(8)FDGPET in anti-AMPA receptor limbic encephalitis. J Neuroimmunol 2014; 271: 53-55
  • 59 Masangkay N, Basu S, Moghbel M. et al. Brain 18F-FDG-PET characteristics in patients with paraneoplastic neurological syndrome and its correlation with clinical and MRI findings. Nucl Med Commun 2014; 35: 1038-1046
  • 60 Fakhoury T, Abou-Khalil B, Kessler RM.. Limbic encephalitis and hyperactive foci on PET scan. Seizure 1999; 8: 427-431
  • 61 Cistaro A, Caobelli F, Quartuccio N. et al. Uncommon 18FFDG-PET/CT findings in patients affected by limbic encephalitis: hyper-hypometabolic pattern with double antibody positivity and migrating foci of hypermetabolism. Clin Imaging 2015; 39: 329-333
  • 62 Thomas AC, Brown RK, Begum R. et al. Autoimmune limbic encephalitis detected on FDG brain scan performed for the evaluation of dementia. Clin Nucl Med 2015; 40: 358-359
  • 63 Santiago MDC, Jurado RS, Llorens RS. et al. Limbic Encephalitis Diagnosed With F-18-FDG PET/CT. Clinical Nuclear Medicine 2016; 41: E101-E103
  • 64 Newey CR, Sarwal A, Hantus S.. [F-18]-Fluoro-Deoxy-Glucose Positron Emission Tomography Scan Should Be Obtained Early in Cases of Autoimmune Encephalitis. Autoimmun Dis 2016;
  • 65 Taneja S, Suri V, Ahuja A. et al. Simultaneous 18F-FDG PET/MRI in Autoimmune Limbic Encephalitis. Indian J Nucl Med 2018; 33: 174-176
  • 66 Deuschl C, Ruber T, Ernst L. et al. F-18-FDG-PET/MRI in the diagnostic work-up of limbic encephalitis. Plos One 2020; 15
  • 67 Morbelli S, Djekidel M, Hesse S. et al. Role of F-18-FDG-PET imaging in the diagnosis of autoimmune encephalitis. Lancet Neurology 2016; 15: 1009-1010
  • 68 Moreno-Ajona D, Prieto E, Grisanti F. et al. 18)F-FDG-PET Imaging Patterns in Autoimmune Encephalitis: Impact of Image Analysis on the Results. Diagnostics (Basel) 2020; 10
  • 69 Seniaray N, Verma R, Ranjan R. et al. Metabolic Imaging Patterns on F-18-FDG PET in Acute and Subacute LGI1 Autoimmune Limbic Encephalitis. Clinical Nuclear Medicine 2021; 46: e27-e28
  • 70 Caquot PA, Zizi G, Lelievre M. et al. F-18-FDG PET/CT in Anti-Leucine-Rich Glioma-Inactivated 1 Antibody Encephalitis Typical Pattern and Follow-up. Clinical Nuclear Medicine 2021; 46: 250-251
  • 71 Vercosa AFA, Mota IA, Flamini MEDD. et al. Paraneoplastic Limbic Encephalitis Secondary to SCLC on F-18-FDG PET/CT. Clinical Nuclear Medicine 2021; 46: 494-496
  • 72 Kim TJ, Lee ST, Shin JW. et al. Clinical manifestations and outcomes of the treatment of patients with GABAB encephalitis. J Neuroimmunol 2014; 270: 45-50
  • 73 Park S, Choi H, Cheon GJ. et al. 18F-FDG PET/CT in anti-LGI1 encephalitis: initial and follow-up findings. Clin Nucl Med 2015; 40: 156-158
  • 74 Cash SS, Larvie M, Dalmau J.. Case records of the Massachusetts General Hospital. Case 34-2011: A 75-year-old man with memory loss and partial seizures. N Engl J Med 2011; 365: 1825-1833
  • 75 Shin YW, Lee ST, Shin JW. et al. VGKC-complex/LGI1-antibody encephalitis: clinical manifestations and response to immunotherapy. J Neuroimmunol 2013; 265: 75-81
  • 76 Basu S, Alavi A.. Role of FDG-PET in the clinical management of paraneoplastic neurological syndrome: detection of the underlying malignancy and the brain PET-MRI correlates. Mol Imaging Biol 2008; 10: 131-137
  • 77 Scheid R, Lincke T, Voltz R. et al. Serial 18F-fluoro-2-deoxy-D-glucose positron emission tomography and magnetic resonance imaging of paraneoplastic limbic encephalitis. Arch Neurol 2004; 61: 1785-1789
  • 78 Ances BM, Vitaliani R, Taylor RA. et al. Treatment-responsive limbic encephalitis identified by neuropil antibodies: MRI and PET correlates. Brain 2005; 128: 1764-1777
  • 79 Chatzikonstantinou A, Szabo K, Ottomeyer C. et al. Successive affection of bilateral temporomesial structures in a case of non-paraneoplastic limbic encephalitis demonstrated by serial MRI and FDG-PET. J Neurol 2009; 256: 1753-1755
  • 80 Kunze A, Drescher R, Kaiser K. et al. Serial FDG PET/CT in autoimmune encephalitis with faciobrachial dystonic seizures. Clin Nucl Med 2014; 39: e436-438
  • 81 Baumgartner A, Rauer S, Mader I. et al. Cerebral FDG-PET and MRI findings in autoimmune limbic encephalitis: correlation with autoantibody types. J Neurol 2013; 260: 2744-2753
  • 82 Endres D, Pruss H, Dressing A. et al. Psychiatric Manifestation of Anti-LGI1 Encephalitis. Brain Sci 2020; 10
  • 83 Borghammer P, Cumming P, Aanerud J. et al. Subcortical elevation of metabolism in Parkinson's disease-a critical reappraisal in the context of global mean normalization. Neuroimage 2009; 47: 1514-1521
  • 84 Barrington SF, Koutroumanidis M, Agathonikou A. et al. Clinical value of „ictal“ FDG-positron emission tomography and the routine use of simultaneous scalp EEG studies in patients with intractable partial epilepsies. Epilepsia 1998; 39: 753-766
  • 85 Fisher RE, Patel NR, Lai EC. et al. Two different 18F-FDG brain PET metabolic patterns in autoimmune limbic encephalitis. Clin Nucl Med 2012; 37: e213-218
  • 86 Leypoldt F, Buchert R, Kleiter I. et al. Fluorodeoxyglucose positron emission tomography in anti-N-methyl-D-aspartate receptor encephalitis: distinct pattern of disease. J Neurol Neurosurg Psychiatry 2012; 83: 681-686
  • 87 Moubtakir A, Dejust S, Godard F. et al. 18F-FDG PET/CT in Anti-NMDA Receptor Encephalitis: Typical Pattern and Follow-up. Clin Nucl Med 2018; 43: 520-521
  • 88 Solnes LB, Jones KM, Rowe SP. et al. Diagnostic Value of (18) F-FDG PET/CT Versus MRI in the Setting of Antibody-Specific Autoimmune Encephalitis. J Nucl Med 2017; 58: 1307-1313
  • 89 Irani SR, Michell AW, Lang B. et al. Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann Neurol 2011; 69: 892-900
  • 90 Boesebeck F, Schwarz O, Dohmen B. et al. Faciobrachial dystonic seizures arise from cortico-subcortical abnormal brain areas. J Neurol 2013; 260: 1684-1686
  • 91 Fidzinski P, Jarius S, Gaebler C. et al. Faciobrachial dystonic seizures and antibodies to Lgi1 in a 92-year-old patient: a case report. J Neurol Sci 2014; 347: 404-405
  • 92 Rey C, Koric L, Guedj E. et al. Striatal hypermetabolism in limbic encephalitis. J Neurol 2012; 259: 1106-1110
  • 93 Bartlett EJ, Brodie JD, Simkowitz P. et al. Effects of haloperidol challenge on regional cerebral glucose utilization in normal human subjects. Am J Psychiatry 1994; 151: 681-686
  • 94 Probasco JC, Solnes L, Nalluri A. et al. Abnormal brain metabolism on FDG-PET/CT is a common early finding in autoimmune encephalitis. Neurol Neuroimmunol Neuroinflamm 2017; 4: e352
  • 95 De Leiris N, Ruel B, Vervandier J. et al. Decrease in the cortex/striatum metabolic ratio on [F-18]-FDG PET: a biomarker of autoimmune encephalitis. Eur J Nucl Med Mol I 2022; 49: 921-931
  • 96 Moloney P, Boylan R, Elamin M. et al. Semi-quantitative analysis of cerebral FDG-PET reveals striatal hypermetabolism and normal cortical metabolism in a case of VGKCC limbic encephalitis. Neuroradiol J 2017; 30
  • 97 Trevino-Peinado C, Arbizu J, Irimia P. et al. Monitoring the effect of immunotherapy in autoimmune limbic encephalitis using 18F-FDG PET. Clin Nucl Med 2015; 40: e441-443
  • 98 Bordonne M, Chawki MB, Doyen M. et al. Brain F-18-FDG PET for the diagnosis of autoimmune encephalitis: a systematic review and a meta-analysis. Eur J Nucl Med Mol I 2021; 48: 3847-3858
  • 99 Guerin J, Watson RE, Carr CM. et al. Autoimmune epilepsy: findings on MRI and FDG-PET. Br J Radiol 2019; 92: 20170869
  • 100 Hadjivassiliou M, Alder SJ, Van Beek EJ. et al. PET scan in clinically suspected paraneoplastic neurological syndromes: a 6-year prospective study in a regional neuroscience unit. Acta Neurol Scand 2009; 119: 186-193
  • 101 Sheikhbahaei S, Marcus CV, Fragomeni RS. et al. Wholebody (18)F-FDG PET and (18)F-FDG PET/CT in patients with suspected paraneoplastic syndrome: A systematic review and meta-analysis of diagnostic accuracy. J Nucl Med 2017; 58: 1031-1036
  • 102 Titulaer MJ, Soffietti R, Dalmau J. et al. Screening for tumours in paraneoplastic syndromes: report of an EFNS task force. Eur J Neurol 2011; 18: 19-e13
  • 103 McKeon A, Apiwattanakul M, Lachance DH. et al. Positron emission tomography-computed tomography in paraneoplastic neurologic disorders: systematic analysis and review. Arch Neurol 2010; 67: 322-329
  • 104 Wegner F, Wilke F, Raab P. et al. Anti-leucine rich glioma inactivated 1 protein and anti-N-methyl-D-aspartate receptor encephalitis show distinct patterns of brain glucose metabolism in 18F-fluoro-2-deoxy-d-glucose positron emission tomography. BMC Neurol 2014; 14: 136
  • 105 Guedj E, Varrone A, Boellaard R. et al. EANM procedure guidelines for brain PET imaging using [F-18]FDG, version 3 (vol 49, pg 632, 2022). Eur J Nucl Med Mol I 2022;
  • 106 Morbelli S, Arbizu J, Booij J. et al. The need of standardization and of large clinical studies in an emerging indication of [(18)F]FDG PET: the autoimmune encephalitis. Eur J Nucl Med Mol Imaging 2017; 44: 353-357