Autoimmune epilepsy: Clinical characteristics and response to immunotherapy

Amy M L Quek, Jeffrey W. Britton, Andrew B McKeon, Elson So, Vanda A Lennon, Cheolsu Shin, Christopher Jon Klein, Robert E. Watson, Amy L. Kotsenas, Terrence D. Lagerlund, Gregory D Cascino, Gregory Alan Worrell, Elaine C Wirrell, Katherine C Nickels, Allen Jr. Aksamit, Katherine H. Noe, Sean J Pittock

Research output: Contribution to journalArticle

193 Citations (Scopus)

Abstract

Objective: To describe clinical characteristics and immunotherapy responses in patients with autoimmune epilepsy. Design: Observational, retrospective case series. Setting: Mayo Clinic Health System. Patients: Thirty-two patients with an exclusive (n=11) or predominant (n=21) seizure presentation in whom an autoimmune etiology was suspected (on the basis of neural autoantibody [91%], inflammatory cerebrospinal fluid [31%], or magnetic resonance imaging suggesting inflammation [63%]) were studied. All had partial seizures: 81% had failed treatment with 2 or more antiepileptic drugs and had daily seizures and 38% had seizure semiologies that were multifocal or changed with time. Head magnetic resonance imaging was normal in 15 (47%) at onset. Electroencephalogram abnormalities included interictal epileptiform discharges in 20; electrographic seizures in 15; and focal slowing in 13. Neural autoantibodies included voltage-gated potassium channel complex in 56% (leucine-rich, glioma-inactivated 1 specific, 14; contactin-associated proteinlike 2 specific, 1); glutamic acid decarboxylase 65 in 22%; collapsin response-mediator protein 5 in 6%; and Ma2, N-methyl-D-aspartate receptor, and ganglionic acetylcholine receptor in 1 patient each. Intervention: Immunotherapy with intravenous methylprednisolone; intravenous immune globulin; and combinations of intravenous methylprednisolone, intravenous immune globulin, plasmapheresis, or cyclophosphamide. Main Outcome Measure: Seizure frequency. Results: After a median interval of 17 months (range, 3-72 months), 22 of 27 (81%) reported improvement postimmunotherapy; 18 were seizure free. The median time from seizure onset to initiating immunotherapy was 4 months for responders and 22 months for nonresponders (P<.05). All voltage-gated potassium channel complex antibody-positive patients reported initial or lasting benefit (P<.05). One voltage-gated potassium channel complex antibody-positive patient was seizure free after thyroid cancer resection; another responded to antiepileptic drug change alone. Conclusion: When clinical and serological clues suggest an autoimmune basis for medically intractable epilepsy, early-initiated immunotherapy may improve seizure outcome.

Original languageEnglish (US)
Pages (from-to)582-593
Number of pages12
JournalArchives of Neurology
Volume69
Issue number5
DOIs
StatePublished - May 2012

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Immunotherapy
Epilepsy
Seizures
Voltage-Gated Potassium Channels
Intravenous Immunoglobulins
Methylprednisolone
Anticonvulsants
Autoantibodies
Contactins
Semaphorin-3A
Magnetic Resonance Imaging
Glutamate Decarboxylase
Plasmapheresis
Antibodies
Cholinergic Receptors
N-Methyl-D-Aspartate Receptors
Thyroid Neoplasms
Leucine
Glioma
Cyclophosphamide

ASJC Scopus subject areas

  • Clinical Neurology
  • Arts and Humanities (miscellaneous)

Cite this

Autoimmune epilepsy : Clinical characteristics and response to immunotherapy. / Quek, Amy M L; Britton, Jeffrey W.; McKeon, Andrew B; So, Elson; Lennon, Vanda A; Shin, Cheolsu; Klein, Christopher Jon; Watson, Robert E.; Kotsenas, Amy L.; Lagerlund, Terrence D.; Cascino, Gregory D; Worrell, Gregory Alan; Wirrell, Elaine C; Nickels, Katherine C; Aksamit, Allen Jr.; Noe, Katherine H.; Pittock, Sean J.

In: Archives of Neurology, Vol. 69, No. 5, 05.2012, p. 582-593.

Research output: Contribution to journalArticle

Quek, Amy M L ; Britton, Jeffrey W. ; McKeon, Andrew B ; So, Elson ; Lennon, Vanda A ; Shin, Cheolsu ; Klein, Christopher Jon ; Watson, Robert E. ; Kotsenas, Amy L. ; Lagerlund, Terrence D. ; Cascino, Gregory D ; Worrell, Gregory Alan ; Wirrell, Elaine C ; Nickels, Katherine C ; Aksamit, Allen Jr. ; Noe, Katherine H. ; Pittock, Sean J. / Autoimmune epilepsy : Clinical characteristics and response to immunotherapy. In: Archives of Neurology. 2012 ; Vol. 69, No. 5. pp. 582-593.
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abstract = "Objective: To describe clinical characteristics and immunotherapy responses in patients with autoimmune epilepsy. Design: Observational, retrospective case series. Setting: Mayo Clinic Health System. Patients: Thirty-two patients with an exclusive (n=11) or predominant (n=21) seizure presentation in whom an autoimmune etiology was suspected (on the basis of neural autoantibody [91{\%}], inflammatory cerebrospinal fluid [31{\%}], or magnetic resonance imaging suggesting inflammation [63{\%}]) were studied. All had partial seizures: 81{\%} had failed treatment with 2 or more antiepileptic drugs and had daily seizures and 38{\%} had seizure semiologies that were multifocal or changed with time. Head magnetic resonance imaging was normal in 15 (47{\%}) at onset. Electroencephalogram abnormalities included interictal epileptiform discharges in 20; electrographic seizures in 15; and focal slowing in 13. Neural autoantibodies included voltage-gated potassium channel complex in 56{\%} (leucine-rich, glioma-inactivated 1 specific, 14; contactin-associated proteinlike 2 specific, 1); glutamic acid decarboxylase 65 in 22{\%}; collapsin response-mediator protein 5 in 6{\%}; and Ma2, N-methyl-D-aspartate receptor, and ganglionic acetylcholine receptor in 1 patient each. Intervention: Immunotherapy with intravenous methylprednisolone; intravenous immune globulin; and combinations of intravenous methylprednisolone, intravenous immune globulin, plasmapheresis, or cyclophosphamide. Main Outcome Measure: Seizure frequency. Results: After a median interval of 17 months (range, 3-72 months), 22 of 27 (81{\%}) reported improvement postimmunotherapy; 18 were seizure free. The median time from seizure onset to initiating immunotherapy was 4 months for responders and 22 months for nonresponders (P<.05). All voltage-gated potassium channel complex antibody-positive patients reported initial or lasting benefit (P<.05). One voltage-gated potassium channel complex antibody-positive patient was seizure free after thyroid cancer resection; another responded to antiepileptic drug change alone. Conclusion: When clinical and serological clues suggest an autoimmune basis for medically intractable epilepsy, early-initiated immunotherapy may improve seizure outcome.",
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AU - Shin, Cheolsu

AU - Klein, Christopher Jon

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AU - Kotsenas, Amy L.

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AU - Cascino, Gregory D

AU - Worrell, Gregory Alan

AU - Wirrell, Elaine C

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N2 - Objective: To describe clinical characteristics and immunotherapy responses in patients with autoimmune epilepsy. Design: Observational, retrospective case series. Setting: Mayo Clinic Health System. Patients: Thirty-two patients with an exclusive (n=11) or predominant (n=21) seizure presentation in whom an autoimmune etiology was suspected (on the basis of neural autoantibody [91%], inflammatory cerebrospinal fluid [31%], or magnetic resonance imaging suggesting inflammation [63%]) were studied. All had partial seizures: 81% had failed treatment with 2 or more antiepileptic drugs and had daily seizures and 38% had seizure semiologies that were multifocal or changed with time. Head magnetic resonance imaging was normal in 15 (47%) at onset. Electroencephalogram abnormalities included interictal epileptiform discharges in 20; electrographic seizures in 15; and focal slowing in 13. Neural autoantibodies included voltage-gated potassium channel complex in 56% (leucine-rich, glioma-inactivated 1 specific, 14; contactin-associated proteinlike 2 specific, 1); glutamic acid decarboxylase 65 in 22%; collapsin response-mediator protein 5 in 6%; and Ma2, N-methyl-D-aspartate receptor, and ganglionic acetylcholine receptor in 1 patient each. Intervention: Immunotherapy with intravenous methylprednisolone; intravenous immune globulin; and combinations of intravenous methylprednisolone, intravenous immune globulin, plasmapheresis, or cyclophosphamide. Main Outcome Measure: Seizure frequency. Results: After a median interval of 17 months (range, 3-72 months), 22 of 27 (81%) reported improvement postimmunotherapy; 18 were seizure free. The median time from seizure onset to initiating immunotherapy was 4 months for responders and 22 months for nonresponders (P<.05). All voltage-gated potassium channel complex antibody-positive patients reported initial or lasting benefit (P<.05). One voltage-gated potassium channel complex antibody-positive patient was seizure free after thyroid cancer resection; another responded to antiepileptic drug change alone. Conclusion: When clinical and serological clues suggest an autoimmune basis for medically intractable epilepsy, early-initiated immunotherapy may improve seizure outcome.

AB - Objective: To describe clinical characteristics and immunotherapy responses in patients with autoimmune epilepsy. Design: Observational, retrospective case series. Setting: Mayo Clinic Health System. Patients: Thirty-two patients with an exclusive (n=11) or predominant (n=21) seizure presentation in whom an autoimmune etiology was suspected (on the basis of neural autoantibody [91%], inflammatory cerebrospinal fluid [31%], or magnetic resonance imaging suggesting inflammation [63%]) were studied. All had partial seizures: 81% had failed treatment with 2 or more antiepileptic drugs and had daily seizures and 38% had seizure semiologies that were multifocal or changed with time. Head magnetic resonance imaging was normal in 15 (47%) at onset. Electroencephalogram abnormalities included interictal epileptiform discharges in 20; electrographic seizures in 15; and focal slowing in 13. Neural autoantibodies included voltage-gated potassium channel complex in 56% (leucine-rich, glioma-inactivated 1 specific, 14; contactin-associated proteinlike 2 specific, 1); glutamic acid decarboxylase 65 in 22%; collapsin response-mediator protein 5 in 6%; and Ma2, N-methyl-D-aspartate receptor, and ganglionic acetylcholine receptor in 1 patient each. Intervention: Immunotherapy with intravenous methylprednisolone; intravenous immune globulin; and combinations of intravenous methylprednisolone, intravenous immune globulin, plasmapheresis, or cyclophosphamide. Main Outcome Measure: Seizure frequency. Results: After a median interval of 17 months (range, 3-72 months), 22 of 27 (81%) reported improvement postimmunotherapy; 18 were seizure free. The median time from seizure onset to initiating immunotherapy was 4 months for responders and 22 months for nonresponders (P<.05). All voltage-gated potassium channel complex antibody-positive patients reported initial or lasting benefit (P<.05). One voltage-gated potassium channel complex antibody-positive patient was seizure free after thyroid cancer resection; another responded to antiepileptic drug change alone. Conclusion: When clinical and serological clues suggest an autoimmune basis for medically intractable epilepsy, early-initiated immunotherapy may improve seizure outcome.

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