FDG-PET-Bildgebung der limbischen Enzephalitis

Ralph Buchert; Sebastian Rauer; Philipp T. Meyer

doi:10.1055/a-1712-6205

Angewandte Nuklearmedizin, Table of Contents

Angewandte Nuklearmedizin 2022; 45(04): 325-344
DOI: 10.1055/a-1712-6205

CME-Fortbildung

FDG-PET-Bildgebung der limbischen Enzephalitis

FDG-PET imaging of limbic encephalitis

Authors

Ralph Buchert
Sebastian Rauer
Philipp T. Meyer

Abstract

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.

Abstract

FDG-PET of the brain provides essential information to support diagnosis, prognosis and therapy monitoring in limbic encephalitis. With increasing attention to limbic encephalitis as „not to miss“ diagnosis, the importance of brain FDG-PET will continue to increase for this indication. Furthermore, whole-body FDG-PET/CT plays a key role in cases of suspected paraneoplastic genesis and unremarkable conventional imaging.

Schlüsselwörter

limbische Enzephalitis - Autoimmunerkrankung - Positronenemissionstomografie - Fluorodesoxyglukose - FDG

Keywords

limbic encephalitis - autoimmune - positron-emission tomography - fluorodeoxyglucose F18 - imaging

Full Text

References

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 antibody-mediated 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 3rd L. et al. Brain on fire: an imaging-based 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)FDG-PET 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 18F-FDG-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. Whole-body (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