Immunotherapy in Autoimmune and Neuroinflammation-Related Epilepsies

Kapil Arya; Erin Willis; Debopam Samanta

doi:10.1055/s-0038-1668589

Journal of Pediatric Epilepsy, Table of Contents

Journal of Pediatric Epilepsy 2018; 07(02): 069-075
DOI: 10.1055/s-0038-1668589

Review Article

Georg Thieme Verlag KG Stuttgart · New York

Immunotherapy in Autoimmune and Neuroinflammation-Related Epilepsies

Kapil Arya

¹Department of Pediatrics, Section of Child Neurology, Arkansas Children's Hospital, University of Arkansas for Medical Sciences, Little Rock, Arkansas, United States

,

Erin Willis

¹Department of Pediatrics, Section of Child Neurology, Arkansas Children's Hospital, University of Arkansas for Medical Sciences, Little Rock, Arkansas, United States

,

Debopam Samanta

¹Department of Pediatrics, Section of Child Neurology, Arkansas Children's Hospital, University of Arkansas for Medical Sciences, Little Rock, Arkansas, United States

› Author Affiliations

Abstract

There is increasing recognition of the role played by neuroinflammation both as a factor in the development of epilepsy as well as a consequence of seizures. Autoimmune encephalitis and epilepsies have emerged as an important etiology of drug-refractory epilepsies. The recognition of these entities is vital for immunomodulation and is the cornerstone in its management. Immunotherapy treatment regimens in these conditions continue to be refined, and there is an increasing knowledge in their use. This article attempts to review the experience with the use of different immunotherapies in specific autoimmune and neuroinflammation-related encephalitis and epilepsies including their mechanisms of action and potential side effects.

Keywords

neuroinflammation - epilepsy - therapy

Full Text

References

References
1 Pernot F, Heinrich C, Barbier L. , et al. Inflammatory changes during epileptogenesis and spontaneous seizures in a mouse model of mesiotemporal lobe epilepsy. Epilepsia 2011; 52 (12) 2315-2325
2 Bauer J, Becker AJ, Elyaman W. , et al. Innate and adaptive immunity in human epilepsies. Epilepsia 2017; 58 (Suppl. 03) 57-68
3 Correll CM. Antibodies in epilepsy. Curr Neurol Neurosci Rep 2013; 13 (05) 348
4 Bien CG. Value of autoantibodies for prediction of treatment response in patients with autoimmune epilepsy: review of the literature and suggestions for clinical management. Epilepsia 2013; 54 (Suppl. 02) 48-55
5 Shin YW, Lee ST, Park KI. , et al. Treatment strategies for autoimmune encephalitis. Ther Adv Neurol Disorder 2017; 11: 1756285617722347
6 Graus F, Titulaer MJ, Balu R. , et al. A clinical approach to diagnosis of autoimmune encephalitis. Lancet Neurol 2016; 15 (04) 391-404
7 Byrne S, Walsh C, Hacohen Y. , et al. Earlier treatment of NMDAR antibody encephalitis in children results in a better outcome. Neurol Neuroimmunol Neuroinflamm 2015; 2 (04) e130
8 Quek AM, Britton JW, McKeon A. , et al. Autoimmune epilepsy: clinical characteristics and response to immunotherapy. Arch Neurol 2012; 69 (05) 582-593
9 Melvin JJ, Huntley Hardison H. Immunomodulatory treatments in epilepsy. Semin Pediatr Neurol 2014; 21 (03) 232-237
10 Witt KA, Sandoval KE. Steroids and the blood-brain barrier: therapeutic implications. Adv Pharmacol 2014; 71: 361-390
11 Tuem KB, Atey TM. Neuroactive steroids: receptor interactions and responses. Front Neurol 2017; 8: 442
12 Wong PH, White KM. Impact of immunoglobulin therapy in pediatric disease: a review of immune mechanisms. Clin Rev Allergy Immunol 2016; 51 (03) 303-314
13 Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006; 313 (5787): 670-673
14 Tackenberg B, Jelcic I, Baerenwaldt A. , et al. Impaired inhibitory Fcgamma receptor IIB expression on B cells in chronic inflammatory demyelinating polyneuropathy. Proc Natl Acad Sci U S A 2009; 106 (12) 4788-4792
15 Samuelsson A, Towers TL, Ravetch JV. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science 2001; 291 (5503): 484-486
16 Jacob S, Rajabally YA. Current proposed mechanisms of action of intravenous immunoglobulins in inflammatory neuropathies. Curr Neuropharmacol 2009; 7 (04) 337-342
17 Durandy A, Kaveri SV, Kuijpers TW. , et al. Intravenous immunoglobulins–understanding properties and mechanisms. Clin Exp Immunol 2009; 158 (Suppl. 01) 2-13
18 Lehmann HC, Hartung HP, Hetzel GR, Stüve O, Kieseier BC. Plasma exchange in neuroimmunological disorders: part 1: rationale and treatment of inflammatory central nervous system disorders. Arch Neurol 2006; 63 (07) 930-935
19 DeSena AD, Noland DK, Matevosyan K. , et al. Intravenous methylprednisolone versus therapeutic plasma exchange for treatment of anti-N-methyl-D-aspartate receptor antibody encephalitis: a retrospective review. J Clin Apher 2015; 30 (04) 212-216
20 Dogan Onugoren M, Golombeck KS, Bien C. , et al. Immunoadsorption therapy in autoimmune encephalitides. Neurol Neuroimmunol Neuroinflamm 2016; 3 (02) e207
21 Lancaster E, Martinez-Hernandez E, Dalmau J. Encephalitis and antibodies to synaptic and neuronal cell surface proteins. Neurology 2011; 77 (02) 179-189
22 Gottenberg JE, Guillevin L, Lambotte O. , et al; Club Rheumatismes et Inflammation (CRI). Tolerance and short term efficacy of rituximab in 43 patients with systemic autoimmune diseases. Ann Rheum Dis 2005; 64 (06) 913-920
23 Hauser SL, Waubant E, Arnold DL. , et al; HERMES Trial Group. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med 2008; 358 (07) 676-688
24 Memon AB, Javed A, Caon C. , et al. Long-term safety of rituximab induced peripheral B-cell depletion in autoimmune neurological diseases. PLoS One 2018; 13 (01) e0190425
25 Lee WJ, Lee ST, Byun JI. , et al. Rituximab treatment for autoimmune limbic encephalitis in an institutional cohort. Neurology 2016; 86 (18) 1683-1691
26 Wang BJ, Wang CJ, Zeng ZL, Yang Y, Guo SG. Lower dosages of rituximab used successfully in the treatment of anti-NMDA receptor encephalitis without tumour. J Neurol Sci 2017; 377: 127-132
27 Winkelstein A. Mechanisms of immunosuppression: effects of cyclophosphamide on cellular immunity. Blood 1973; 41 (02) 273-284
28 McKeon A. Immunotherapeutics for autoimmune encephalopathies and dementias. Curr Treat Options Neurol 2013; 15 (06) 723-737
29 Carreño M, Bien CG, Asadi-Pooya AA. , et al. Epilepsy surgery in drug resistant temporal lobe epilepsy associated with neuronal antibodies. Epilepsy Res 2017; 129: 101-105
30 Scheibe F, Prüss H, Mengel AM. , et al. Bortezomib for treatment of therapy-refractory anti-NMDA receptor encephalitis. Neurology 2017; 88 (04) 366-370
31 Lee WJ, Lee ST, Moon J. , et al. Tocilizumab in autoimmune encephalitis refractory to rituximab: an institutional cohort study. Neurotherapeutics 2016; 13 (04) 824-832
32 Brenton JN, Kim J, Schwartz RH. Approach to the management of pediatric-onset anti-N-methyl-D-aspartate (anti-NMDA) receptor encephalitis: a case series. J Child Neurol 2016; 31 (09) 1150-1155
33 Zhang L, Wu MQ, Hao ZL. , et al. Clinical characteristics, treatments, and outcomes of patients with anti-N-methyl-D-aspartate receptor encephalitis: a systematic review of reported cases. Epilepsy Behav 2017; 68: 57-65
34 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. Lancet Neurol 2013; 12 (02) 157-165
35 Bartolini L, Muscal E. Differences in treatment of anti-NMDA receptor encephalitis: results of a worldwide survey. J Neurol 2017; 264 (04) 647-653
36 Herranz-Pérez V, Olucha-Bordonau FE, Morante-Redolat JM, Pérez-Tur J. Regional distribution of the leucine-rich glioma inactivated (LGI) gene family transcripts in the adult mouse brain. Brain Res 2010; 1307: 177-194
37 Lovero KL, Fukata Y, Granger AJ, Fukata M, Nicoll RA. The LGI1-ADAM22 protein complex directs synapse maturation through regulation of PSD-95 function. Proc Natl Acad Sci U S A 2015; 112 (30) E4129-E4137
38 Fukata Y, Lovero KL, Iwanaga T. , et al. Disruption of LGI1-linked synaptic complex causes abnormal synaptic transmission and epilepsy. Proc Natl Acad Sci U S A 2010; 107 (08) 3799-3804
39 Kalachikov S, Evgrafov O, Ross B. , et al. Mutations in LGI1 cause autosomal-dominant partial epilepsy with auditory features. Nat Genet 2002; 30 (03) 335-341
40 Lai M, Huijbers MG, Lancaster E. , et al. Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol 2010; 9 (08) 776-785
41 Andrade DM, Tai P, Dalmau J, Wennberg R. Tonic seizures: a diagnostic clue of anti-LGI1 encephalitis?. Neurology 2011; 76 (15) 1355-1357
42 Irani SR, Michell AW, Lang B. , et al. Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann Neurol 2011; 69 (05) 892-900
43 Kotsenas AL, Watson RE, Pittock SJ. , et al. MRI findings in autoimmune voltage-gated potassium channel complex encephalitis with seizures: one potential etiology for mesial temporal sclerosis. Am J Neuroradiol 2014; 35 (01) 84-89
44 Ariño H, Armangué T, Petit-Pedrol M. , et al. Anti-LGI1-associated cognitive impairment: presentation and long-term outcome. Neurology 2016; 87 (08) 759-765
45 Bhardwaj K, Sharma SK, Pandey AK, Upadhyay V. A case of limbic encephalitis: antibody LGI1 associated encephalitis. J Neurol Neurosci. 2016; 7: 4 . doi: 10.21767/2171-6625.1000137
46 Szots M, Marton A, Kover F. , et al. Natural course of LGI1 encephalitis: 3-5 years of follow-up without immunotherapy. J Neurol Sci 2014; 343 (1–2): 198-202
47 Finke C, Prüss 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 (01) 50-59
48 Manto MU, Laute MA, Aguera M, Rogemond V, Pandolfo M, Honnorat J. Effects of anti-glutamic acid decarboxylase antibodies associated with neurological diseases. Ann Neurol 2007; 61 (06) 544-551
49 Sloviter RS, Dichter MA, Rachinsky TL. , et al. Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 1996; 373 (04) 593-618
50 Daif A, Lukas RV, Issa NP. , et al. Antiglutamic acid decarboxylase 65 (GAD65) antibody-associated epilepsy. Epilepsy Behav 2018; 80: 331-336
51 Malter MP, Frisch C, Zeitler H. , et al. Treatment of immune-mediated temporal lobe epilepsy with GAD antibodies. Seizure 2015; 30: 57-63
52 Saidha S, Murphy S, Ronayne A, McCarthy P, Hennessy MJ, Counihan T. Treatment of anti-glutamic acid decarboxylase antibody-associated limbic encephalitis with mycophenolate mofetil. J Neurol 2010; 257 (06) 1035-1038
53 Lilleker JB, Biswas V, Mohanraj R. Glutamic acid decarboxylase (GAD) antibodies in epilepsy: diagnostic yield and therapeutic implications. Seizure 2014; 23 (08) 598-602
54 Holzer FJ, Rossetti AO, Heritier-Barras AC. , et al. Antibody-mediated status epilepticus: a retrospective multicenter survey. Eur Neurol 2012; 68 (05) 310-317
55 Khawaja AM, Vines BL, Miller DW, Szaflarski JP, Amara AW. Refractory status epilepticus and glutamic acid decarboxylase antibodies in adults: presentation, treatment and outcomes. Epileptic Disord 2016; 18 (01) 34-43
56 Heiry M, Afra P, Matsuo F, Greenlee JE, Clardy SL. Improvement of GAD65-associated autoimmune epilepsy with testosterone replacement therapy. Neurol Neuroimmunol Neuroinflamm 2015; 2 (05) e142
57 Bien CG, Granata T, Antozzi C. , et al. Pathogenesis, diagnosis and treatment of Rasmussen encephalitis: a European consensus statement. Brain 2005; 128 (Pt 3): 454-471
58 Pardo CA, Vining EPG, Guo L, Skolasky RL, Carson BS, Freeman JM. The pathology of Rasmussen syndrome: stages of cortical involvement and neuropathological studies in 45 hemispherectomies. Epilepsia 2004; 45 (05) 516-526
59 Farrell MA, DeRosa MJ, Curran JG. , et al. Neuropathologic findings in cortical resections (including hemispherectomies) performed for the treatment of intractable childhood epilepsy. Acta Neuropathol 1992; 83 (03) 246-259
60 Farrell MA, Droogan O, Secor DL, Poukens V, Quinn B, Vinters HV. Chronic encephalitis associated with epilepsy: immunohistochemical and ultrastructural studies. Acta Neuropathol 1995; 89 (04) 313-321
61 Ransohoff RM, Perry VH. Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 2009; 27: 119-145
62 Bien CG, Bauer J, Deckwerth TL. , et al. Destruction of neurons by cytotoxic T cells: a new pathogenic mechanism in Rasmussen's encephalitis. Ann Neurol 2002; 51 (03) 311-318
63 Rogers SW, Andrews PI, Gahring LC. , et al. Autoantibodies to glutamate receptor GluR3 in Rasmussen's encephalitis. Science 1994; 265 (5172): 648-651
64 Alvarez-Barón E, Bien CG, Schramm J, Elger CE, Becker AJ, Schoch S. Autoantibodies to Munc18, cerebral plasma cells and B-lymphocytes in Rasmussen encephalitis. Epilepsy Res 2008; 80 (01) 93-97
65 Yang R, Puranam RS, Butler LS. , et al. Autoimmunity to munc-18 in Rasmussen's encephalitis. Neuron 2000; 28 (02) 375-383
66 Walter GF, Renella RR. Epstein-Barr virus in brain and Rasmussen's encephalitis. Lancet 1989; 1 (8632): 279-280
67 Power C, Poland SD, Blume WT, Girvin JP, Rice GP. Cytomegalovirus and Rasmussen's encephalitis. Lancet 1990; 336 (8726): 1282-1284
68 Vinters HV, Wang R, Wiley CA. Herpesviruses in chronic encephalitis associated with intractable childhood epilepsy. Hum Pathol 1993; 24 (08) 871-879
69 Vining EP, Freeman JM, Pillas DJ. , et al. Why would you remove half a brain? The outcome of 58 children after hemispherectomy-the Johns Hopkins experience: 1968 to 1996. Pediatrics 1997; 100 (2 Pt 1): 163-171
70 Devlin AM, Cross JH, Harkness W. , et al. Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence. Brain 2003; 126 (Pt 3): 556-566
71 Griessenauer CJ, Salam S, Hendrix P. , et al. Hemispherectomy for treatment of refractory epilepsy in the pediatric age group: a systematic review. J Neurosurg Pediatr 2015; 15 (01) 34-44
72 Andrews PI, Dichter MA, Berkovic SF, Newton MR, McNamara JO. Plasmapheresis in Rasmussen's encephalitis. 1996. Neurology 2001; 57 (11) (Suppl. 04) S37-S41
73 Antozzi C, Granata T, Aurisano N. , et al. Long-term selective IgG immuno-adsorption improves Rasmussen's encephalitis. Neurology 1998; 51 (01) 302-305
74 Thilo B, Stingele R, Knudsen K. , et al. A case of Rasmussen encephalitis treated with rituximab. Nat Rev Neurol 2009; 5 (08) 458-462
75 Maria BL, Ringdahl DM, Mickle JP. , et al. Intraventricular alpha interferon therapy for Rasmussen's syndrome. Can J Neurol Sci 1993; 20 (04) 333-336
76 Granata T, Fusco L, Gobbi G. , et al. Experience with immunomodulatory treatments in Rasmussen's encephalitis. Neurology 2003; 61 (12) 1807-1810
77 van Baalen A, Häusler M, Boor R. , et al. Febrile infection-related epilepsy syndrome (FIRES): a nonencephalitic encephalopathy in childhood. Epilepsia 2010; 51 (07) 1323-1328
78 van Baalen A, Häusler M, Plecko-Startinig B. , et al. Febrile infection-related epilepsy syndrome without detectable autoantibodies and response to immunotherapy: a case series and discussion of epileptogenesis in FIRES. Neuropediatrics 2012; 43 (04) 209-216
79 Kramer U, Chi CS, Lin KL. , et al. Febrile infection-related epilepsy syndrome (FIRES): pathogenesis, treatment, and outcome: a multicenter study on 77 children. Epilepsia 2011; 52 (11) 1956-1965
80 Kenney-Jung DL, Vezzani A, Kahoud RJ. , et al. Febrile infection-related epilepsy syndrome treated with anakinra. Ann Neurol 2016; 80 (06) 939-945
81 Ismail FY, Kossoff EH. AERRPS, DESC, NORSE, FIRES: multi-labeling or distinct epileptic entities?. Epilepsia 2011; 52 (11) e185-e189
82 Gall CR, Jumma O, Mohanraj R. Five cases of new onset refractory status epilepticus (NORSE) syndrome: outcomes with early immunotherapy. Seizure 2013; 22 (03) 217-220
83 Li J, Saldivar C, Maganti RK. Plasma exchange in cryptogenic new onset refractory status epilepticus. Seizure 2013; 22 (01) 70-73