Temporal lobe cortical pathology and inhibitory GABA interneuron cell loss are associated with seizures in multiple sclerosis

Multiple Sclerosis

Volumn 22, Issue 1, 2016, Pages 25-35

  Nicholas, Richard ^a   Magliozzi, Roberta ^a,b   Campbell, Graham ^c   Mahad, Don ^c,d   Reynolds, Richard ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

epilepsy; Multiple sclerosis; neuropathology; seizure; temporal lobe

Indexed keywords

4 AMINOBUTYRIC ACID; CARBAMAZEPINE; CYTOCHROME C OXIDASE; LAMOTRIGINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PHENOBARBITAL; PHENYTOIN; VALPROIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; SUCCINATE DEHYDROGENASE;

4 AMINOBUTYRIC ACID BRAIN LEVEL; ABSCESS; ADULT; AGED; ARTICLE; BRAIN CORTEX ATROPHY; BUTTOCK; CD3+ T LYMPHOCYTE; CELL LOSS; CHEST INFECTION; CHILD; CONFUSION; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DEATH; DISEASE ASSOCIATION; DISEASE DURATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTROENCEPHALOGRAPHY; EPILEPSY; EXPANDED DISABILITY STATUS SCALE; FEMALE; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; GENERALIZED EPILEPSY; GRAY MATTER; HUMAN; HUMAN CELL; HUMAN TISSUE; INCIDENCE; INFLAMMATORY CELL; INTERNEURON; MAJOR CLINICAL STUDY; MALE; MIDDLE TEMPORAL GYRUS; MITOCHONDRION; MULTIPLE SCLEROSIS; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; PRIMARY MOTOR CORTEX; RECURRENT INFECTION; RESPIRATORY CHAIN; SEIZURE; SEPSIS; SUPERIOR FRONTAL GYRUS; TEMPORAL LOBE EPILEPSY; TONIC CLONIC SEIZURE; UNITED KINGDOM; URINARY TRACT INFECTION; WHEELCHAIR; BRAIN CORTEX; COMPLICATION; MIDDLE AGED; PATHOLOGY; SEIZURES; TEMPORAL LOBE; TISSUE BANK; BRAIN ELECTROPHYSIOLOGY; CONCURRENT INFECTION; CONVULSION; DEMYELINATING DISEASE; DISEASE PREDISPOSITION; ENZYME HISTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; QUANTITATIVE ANALYSIS; TEMPORAL CORTEX;

ADULT; AGED; CEREBRAL CORTEX; FEMALE; GABAERGIC NEURONS; HUMANS; INTERNEURONS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; SEIZURES; TEMPORAL LOBE; TISSUE BANKS; UNITED KINGDOM;

EID: 84951082706     PISSN: 13524585     EISSN: 14770970     Source Type: Journal    
DOI: 10.1177/1352458515579445     Document Type: Article

References (35)

1. Williams GH Jr, Nosik W, Hunter J,. Convulsions as manifestation of multiple sclerosis. JAMA 1952; 150: 990-992.
2. Kelley BJ, Rodriguez M,. Seizures in patients with multiple sclerosis: Epidemiology, pathophysiology and management. CNS Drugs 2009; 23: 805-815.
3. Olafsson E, Benedikz J, Hauser WA,. Risk of epilepsy in patients with multiple sclerosis: A population-based study in Iceland. Epilepsia 1999; 40: 745-747.
4. Poser CM, Brinar VV,. Epilepsy and multiple sclerosis. Epilepsy Behav 2003; 4: 6-12.
5. Engelsen BA, Grønning M,. Epileptic seizures in patients with multiple sclerosis. Is the prognosis of epilepsy underestimated? Seizure 1997; 6: 377-382.
6. Koch M, Uyttenboogaart M, Polman S, et al. Seizures in multiple sclerosis. Epilepsia 2008; 49: 948-953.
7. Martínez-Juárez IE, López-Meza E, González-Aragón Mdel C, et al. Epilepsy and multiple sclerosis: Increased risk among progressive forms. Epilepsy Res 2009; 84: 250-253.
8. Nicoletti A, Sofia V, Biondi R, et al. Epilepsy and multiple sclerosis in Sicily: A population-based study. Epilepsia 2003; 44: 1445-1448.
9. Nyquist P, Cascino GD, McClelland RL, et al. Incidence of seizures in patients with multiple sclerosis: A population-based study. Mayo Clin Proc 2002; 77: 910-912.
10. Moreau T, Sochurkova D, Lemesle M, et al. Epilepsy in patients with multiple sclerosis: Radiological-clinical correlations. Epilepsia 1998; 39: 893-896.
11. Schuele SU, Kellinghaus C, Shook SJ, et al. Incidence of seizures in patients with multiple sclerosis treated with intrathecal baclofen. Neurology 2005; 64: 1086-1087.
12. ILAE Commission Report. The epidemiology of the epilepsies: Future directions. International League Against Epilepsy. Epilepsia 1997; 38: 614-618.
13. Kutzelnigg A, Lucchinetti CF, Stadelmann C, et al. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 2005; 128: 2705-2712.
14. Stadelmann C, Albert M, Wegner C, et al. Cortical pathology in multiple sclerosis. Curr Opin Neurol 2008; 21: 229-234.
15. Martínez-Lapiscina EH, Ayuso T, Lacruz F, et al. Cortico-juxtacortical involvement increases risk of epileptic seizures in multiple sclerosis. Acta Neurol Scand 2013; 128: 24-31.
16. Thompson AJ, Kermode AG, Moseley IF, et al. Seizures due to multiple sclerosis: Seven patients with MRI correlations. J Neurol Neurosurg Psychiatry 1993; 56: 1317-1320.
17. Truyen L, Barkhof F, Frequin ST, et al. Magnetic resonance imaging of epilepsy in multiple sclerosis: A case control study. Implications for treatment trials with 4-aminopyridine. Mult Scler 1996; 1: 213-217.
18. Calabrese M, Grossi P, Favaretto A, et al. Cortical pathology in multiple sclerosis patients with epilepsy: A 3 year longitudinal study. J Neurol Neurosurg Psychiatry 2012; 83: 49-54.
19. Dutta R, McDonough J, Yin X, et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 2006; 59: 478-489.
20. Magliozzi R, Howell OW, Roncaroli F, et al. Substantial neuronal loss in the grey matter accompanies the presence of meningeal B-cell follicles in multiple sclerosis. Ann Neurol 2010; 68: 477-493.
21. Allen I, Gentleman S, Graeber M, et al. International Classification of Diseases of the Nervous System-Demyelinating Diseases-Multiple Sclerosis., www.icdns.org/forums (2006,. Accessed: 23 December 2014).
22. Reynolds R, Nicholas R, Roncaroli F, et al. The neuropathological basis of clinical progression in multiple sclerosis. Acta Neuropathol 2011; 17: 1211-1217.
23. Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 1989; 30: 389-399.
24. Choi S, Howell OW, Carassiti D, et al. Does meningeal inflammation play a role in the pathology of primary progressive multiple sclerosis? Brain 2012; 135: 2925-2937.
25. Peterson JW, Bö L, Mörk S, et al. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann Neurol 2001; 50: 389-400.
26. Campbell GR, Ziabreva I, Reeve AK, et al. Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann Neurol 2011; 69: 481-492.
27. Scalfari A, Neuhaus A, Degenhardt A, et al. The natural history of multiple sclerosis: A geographically based study 10: Relapses and long-term disability. Brain 2010; 133: 1914-1929.
28. Hurwitz BJ,. Analysis of current multiple sclerosis registries. Neurology 2011; 76 (Suppl 1): S7-S13.
29. Tremlett H, Paty D, Devonshire V,. Disability progression in multiple sclerosis is slower than previously reported. Neurology 2006; 66: 172-177.
30. Weinshenker BG, Rice GPA, Noseworthy JH, et al. The natural history of multiple sclerosis: A geographically based study. I. Clinical course and disability. Brain 1989; 112: 133-146.
31. Larner AJ,. Epileptic seizures in AD patients. Neuromolecular Med 2010; 12: 71-77.
32. Muzzi P, Camera P, Di Cunto F, et al. Deletion of the citron kinase gene selectively affects the number and distribution of interneurons in barrelfield cortex. J Comp Neurol 2009; 513: 249-264.
33. Waldbaum S, Patel M,. Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res 2010; 88: 23-45.
34. Perry VH, Cunningham C, Holmes C,. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol 2007; 7: 161-167.
35. Kang JQ, Shen W, Macdonald R,. The GABRG2 mutation, Q351X, associated with generalized epilepsy with febrile seizures plus, has both loss of function and dominant-negative suppression. J Neurosci 2009; 29: 2845-2856.