Epileptogenesis after prolonged febrile seizures: Mechanisms, biomarkers and therapeutic opportunities

Neuroscience Letters

Volumn 497, Issue 3, 2011, Pages 155-162

  McClelland, Shawn ^a,b   Dubé, Céline M ^a,b   Yang, Jaqueline ^a,b   Baram, Tallie Z ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biomarkers; Epileptogenesis; Febrile seizures; Gene expression; Inflammation

Indexed keywords

INTERLEUKIN 1BETA;

CELL LOSS; CHILD; CORTICAL DYSPLASIA; DISEASE ASSOCIATION; DISEASE DURATION; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; FEBRILE CONVULSION; GENE EXPRESSION; GENE MUTATION; HUMAN; INFLAMMATION; LEUKOCYTE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVIEW; TEMPORAL LOBE EPILEPSY;

ANIMALS; BIOLOGICAL MARKERS; BRAIN; HUMANS; SEIZURES; SEIZURES, FEBRILE;

EID: 79957858597     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2011.02.032     Document Type: Review

References (131)

1. Alheim K., Bartfai T. The interleukin-1 system: receptors, ligands, and ICE in the brain and their involvement in the fever response, Ann. N. Y. Acad. Sci. 1998, 840:51-58.
2. Annegers J.F., Hauser W.A., Shirts S.B., Kurland L.T. Factors prognostic of unprovoked seizures after febrile convulsions. N. Engl. J. Med. 1987, 316:493-498.
3. Audenaert D., Schwartz E., Claeys K.G., Claes L., Deprez L., Suls A., Van Dyck T., Lagae L., Van Broeckhoven C., Macdonald R.L., De Jonghe P. A novel GABRG2 mutation associated with febrile seizures. Neurology 2006, 67:687-690.
4. Barela A.J., Waddy S.P., Lickfett J.G., Hunter J., Anido A., Helmers S.L., Goldin A.L., Escayg A. An epilepsy mutation in the sodium channel SCN1A that decreases channel excitability. J. Neurosci. 2006, 26:2714-2723.
5. Barone S.R., Kaplan M.H., Krilov L.R. Human herpesvirus-6 infection in children with first febrile seizures. J. Pediatr. 1995, 127:95-97.
6. Bassuk A.G., Wallace R.H., Buhr A., Buller A.R., Afawi Z., Shimojo M., Miyata S., Chen S., Gonzalez-Alegre P., Griesbach H.L., Wu S., Nashelsky M., Vladar E.K., Antic D., Ferguson P.J., Cirak S., Voit T., Scott M.P., Axelrod J.D., Gurnett C., Daoud A.S., Kivity S., Neufeld M.Y., Mazarib A., Straussberg R., Walid S., Korczyn A.D., Slusarski D.C., Berkovic S.F., El-Shanti H.I. A homozygous mutation in human PRICKLE1 causes an autosomal-recessive progressive myoclonus epilepsy-ataxia syndrome. Am. J. Hum. Genet. 2008, 83:572-581.
7. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985, 14:375-403.
8. Ben-Ari Y., Holmes G.L. Effects of seizures on developmental processes in the immature brain. Lancet Neurol. 2006, 5:1055-1063.
9. Bender R.A., Dubé C., Gonzalez-Vega R., Mina E.W., Baram T.Z. Mossy fiber plasticity and enhanced hippocampal excitability, without hippocampal cell loss or altered neurogenesis, in an animal model of prolonged febrile seizures. Hippocampus 2003, 13:399-412.
10. Bender R.A, Soleymani S.V., Brewster A.L., Nguyen S.T., Beck H., Mathern G.W., Baram T.Z. Enhanced expression of a specific hyperpolarization-activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus. J. Neurosci. 2003, 23:6826-6836.
11. Berg A.T., Shinnar S. Unprovoked seizures in children with febrile seizures: short-term outcome. Neurology 1996, 47:562-568.
12. Berg A.T., Shinnar S. Complex febrile seizures. Epilepsia 1996, 37:126-133.
13. Berg A.T., Shinnar S., Shapiro E.D., Salomon M.E., Crain E.F., Hauser W.A. Risk factors for a first febrile seizure: a matched case-control study. Epilepsia 1995, 36:334-341.
14. Berg A.T., Shinnar S., Darefsky A.S., Holford T.R., Shapiro E.D., Salomon M.E., Crain E.F., Hauser A.W. Predictors of recurrent febrile seizures: a prospective cohort study. Arch. Pediatr. Adolesc. Med. 1997, 151:371-378.
15. Berg A.T., Shinnar S., Levy S.R., Testa F.M. Childhood-onset epilepsy with and without preceding febrile seizures. Neurology 1999, 53:1742-1748.
16. Berkovic S., Scheffer I. Febrile seizures: genetics and relationship to other epilepsy syndromes. Curr. Opin. Neurol. 1998, 11:129-134.
17. Bethune P., Gordon K., Dooley J., Camfield C., Camfield P.I. Which child will have a febrile seizure?. Am. J. Dis. Child. 1993, 147:35-39.
18. Bien C.G., Urbach H., Schramm J., Soeder B.M., Becker A.J., Voltz R., Vincent A., Elger C.E. Limbic encephalitis as a precipitating event in adult-onset temporal lobe epilepsy. Neurology 2007, 69:1236-1244.
19. Boer K., Crino P.B., Gorter J.A., Nellist M., Jansen F.E., Spliet W.G., van Rijen P.C., Wittink F.R., Breit T.M., Troost D., Wadman W.J., Aronica E. Gene expression analysis of tuberous sclerosis complex cortical tubers reveals increased expression of adhesion and inflammatory factors. Brain Pathol. 2010, 20:704-719.
20. Bowser D.N., Wagner D.A., Czajkowski C., Cromer B.A., Parker M.W., Wallace R.H., Harkin L.A., Mulley J.C., Marini C., Berkovic S.F., Williams D.A., Jones M.V., Petrou S. Altered kinetics and benzodiazepine sensitivity of a GABAA receptor subunit mutation [gamma 2(R43Q)] found in human epilepsy. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15170-15175.
21. Brewster A.L., Bender R.A., Chen Y., Dube C., Eghbal-Ahmadi M., Baram T.Z. Developmental febrile seizures modulate hippocampal gene expression of hyperpolarization-activated channels in an isoform- and cell-specific manner. J. Neurosci. 2002, 22:4591-4599.
22. Brewster A.L., Bernard J.A., Gall C.M., Baram T.Z. Formation of heteromeric hyperpolarization-activated cyclic nucleotide-gated (HCN) channels in the hippocampus is regulated by developmental seizures. Neurobiol. Dis. 2005, 19:200-207.
23. Camfield P., Camfield C. Febrile seizures. Childhood Seizures 1995, 32-38. Karger, Basel. S. Shinnar, N. Amir, D. Branski (Eds.).
24. Cartmell T., Luheshi G.N., Rothwell N.J. Brain sites of action of endogenous interleukin-1 in the febrile response to localized inflammation in the rat. J. Physiol. 1999, 518:585-594.
25. Cassano P.A., Koepsell T.D., Farwell J.R. Risk of febrile seizures in childhood in relation to prenatal maternal cigarette smoking and alcohol intake. Am. J. Epidemiol. 1990, 132:462-473.
26. Cendes F., Andermann F., Dubeau F., Gloor P., Evans A., Jones-Gotman M., Olivier A., Andermann E., Robitaille Y., Lopes-Cendes I., Peters T., Melanson D. Early childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study. Neurology 1993, 43:1083-1087.
27. Chang Y.C, Huang A.M., Kuo Y.M., Wang S.T., Chang Y.Y., Huang C.C. Febrile seizures impair memory and cAMP response-element binding protein activation. Ann. Neurol. 2003, 54:706-718.
28. Chang Y.C., Kuo Y.M., Huang A.M., Huang C.C. Repetitive febrile seizures in rat pups cause long-lasting deficits in synaptic plasticity and NR2A tyrosine phosphorylation. Neurobiol. Dis. 2005, 18:466-475.
29. Chen K., Baram T.Z., Soltesz I. Febrile seizures in the developing brain result in persistent modification of neuronal excitability in limbic circuits. Nat. Med. 1999, 5:888-894.
30. Chen K., Aradi I., Thon N., Eghbal-Ahmadi M., Baram T.Z., Soltesz I. Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nat. Med. 2001, 7:331-337.
31. Chen K., Ratzliff A., Hilgenberg L., Gulyás A., Freund T.F., Smith M., Dinh T.P., Piomelli D., Mackie K., Soltesz I. Long-term plasticity of endocannabinoid signaling induced by developmental febrile seizures. Neuron 2003, 39:599-611.
32. Chen K., Neu A., Howard A.L., Földy C., Echegoyen J., Hilgenberg L., Smith M., Mackie K., Soltesz I. Prevention of plasticity of endocannabinoid signaling inhibits persistent limbic hyperexcitability caused by developmental seizures. J. Neurosci. 2007, 27:46-58.
33. Chisholm J., Kellogg C., Franck J.E. Developmental hyperthermic seizures alter adult hippocampal benzodiazepine binding and morphology. Epilepsia 1985, 26:151-157.
34. de Lanerolle N.C., Kim J.H., Robbins R.J., Spencer D.D. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 1989, 495:387-395.
35. Dibbens L.M., Reid C.A., Hodgson B., Thomas E.A., Phillips A.M., Gazina E., Cromer B.A., Clarke A.L., Baram T.Z., Scheffer I.E., Berkovic S.F., Petrou S. Augmented currents of an HCN2 variant in patients with febrile seizure syndromes. Ann. Neurol. 2010, 67:542-546.
36. Dubé C., Chen K., Eghbal-Ahmad M., Brunson K., Soltesz I., Baram T.Z. Prolonged febrile seizures in the immature rat model enhance hippocampal excitability long-term. Ann. Neurol. 2000, 47:336-344.
37. Dubé C., Yu H., Nalcioglu O., Baram T.Z. Serial MRI after experimental febrile seizures: altered T2 signal without neuronal death. Ann. Neurol. 2004, 56:709-714.
38. Dubé C., Brunson K.L., Eghbal-Ahmadi M., Gonzalez-Vega R., Baram T.Z. Endogenous neuropeptide Y prevents recurrence of experimental febrile seizures by increasing seizure threshold. J. Mol. Neurosci. 2005, 25:275-284.
39. Dubé C., Vezzani A., Behrens M., Bartfai T., Baram T.Z. Interleukin-1β contributes to the generation of experimental febrile seizures. Ann. Neurol. 2005, 57:152-155.
40. Dubé C., Richichi C., Bender R.A., Chung G., Litt B., Baram T.Z. Temporal lobe epilepsy after experimental prolonged febrile seizures: prospective analysis. Brain 2006, 129:911-922.
41. Dubé C.M., Brewster A.L., Richichi C., Zha Q., Baram T.Z. Fever, febrile seizures and epilepsy. Trends Neurosci. 2007, 30:490-496.
42. Dubé C.M., Brewster A.L., Baram T.Z. Febrile seizures: mechanisms and relationship to epilepsy. Brain Dev. 2009, 31:366-371.
43. Dubé C.M., Zhou J.L., Hamamura M., Zhao Q., Ring A., Abrahams J., McIntyre K., Nalcioglu O., Shatskih T., Baram T.Z., Holmes G.L. Cognitive dysfunction after experimental febrile seizures. Exp. Neurol. 2009, 215:167-177.
44. Dubé C.M., Ravizza T., Hamamura M., Zha Q., Keebaugh A., Fok K., Andres A.L., Nalcioglu O., Obenaus A., Vezzani A., Baram T.Z. Epileptogenesis provoked by prolonged experimental febrile seizures: mechanisms and biomarkers. J. Neurosci. 2010, 30:7484-7494.
45. Dugladze T., Vida I., Tort A.B., Gross A., Otahal J., Heinemann U., Kopell N.J., Gloveli T. Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17530-17535.
46. Escayg A., MacDonald B.T., Meisler M.H., Baulac S., Huberfeld G., An-Gourfinkel I., Brice A., LeGuern E., Moulard B., Chaigne D., Buresi C., Malafosse A. Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat. Genet. 2000, 24:343-345.
47. Forsgren L., Sidenvall R., Blomquist H.K., Heijbel J., Nyström L. An incident case-referent study of febrile convulsions in children: genetical social aspects. Neuropediatrics 1990, 21:153-159.
48. Fotheringham J., Donati D., Akhyani N., Fogdell-Hahn A., Vortmeyer A., Heiss J.D., Williams E., Weinstein S., Bruce D.A., Gaillard W.D., Sato S., Theodore W.H., Jacobson S. Association of human herpesvirus-6B with mesial temporal lobe epilepsy. PLoS Med. 2007, 5:e180.
49. Frantzen E., Lennox-Buchthal M., Nygaard A. Longitudinal EEG and clinical study of children with febrile convulsions. Electroencephalogr. Clin. Neurophysiol. 1968, 24:197-212.
50. French J.A., Williamson P.D., Thadani V.M., Darcey T.M., Mattson R.H., Spencer S.S., Spencer D.D. Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann. Neurol. 1993, 34:774-780.
51. Germano I.M., Zhang Y.F., Sperber E.F., Moshé S.L. Neuronal migration disorders increase susceptibility to hyperthermia-induced seizures in developing rats. Epilepsia 1996, 37:902-910.
52. Gillies S.G., Haddley K., Vasiliou S.A., Jacobson G.M., von Mentzer B., Bubb V.J., Quinn J.P. Distinct gene expression profiles directed by the isoforms of the transcription factor neuron-restrictive silencer factor in human SK-N-AS neuroblastoma cells. J. Mol. Neurosci. 2010, (July).
53. Goodkin H.P., Joshi S., Mtchedlishvili Z., Brar J., Kapur J. Subunit-specific trafficking of GABA(A) receptors during status epilepticus. J. Neurosci. 2008, 28:2527-2538.
54. Hamati-Haddad A., Abou-Khalil B. Epilepsy diagnosis and localization in patients with antecedent childhood febrile convulsions. Neurology 1998, 50:917-922.
55. Harkin L.A., Bowser D.N., Dibbens L.M., Singh R., Phillips F., Wallace R.H., Richards M.C., Williams D.A., Mulley J.C., Berkovic S.F., Scheffer I.E., Petrou S. Truncation of the GABA(A)-receptor gamma2 subunit in a family with generalized epilepsy with febrile seizures plus. Am. J. Hum. Genet. 2002, 70:530-536.
56. Haspolat S., Mihçi E., Coskun M., Gümüslü S., Ozben T., Yegin O. Interleukin-1beta, tumor necrosis factor-alpha, and nitrite levels in febrile seizures. J. Child Neurol. 2002, 17:749-751.
57. Hatalski C.G., Brunson K.L., Tantayanubutr B., Chen Y., Baram T.Z. Neuronal activity and stress differentially regulate hippocampal and hypothalamic corticotropin-releasing hormone expression in the immature rat. Neuroscience 2000, 101:571-580.
58. Heida J.G., Pittman Q.J. Causal links between brain cytokines and experimental febrile convulsions in the rat. Epilepsia 2005, 46:1906-1913.
59. Houser C.R. Neuronal loss and synaptic reorganization in temporal lobe epilepsy. Adv. Neurol. 1999, 79:743-761.
60. Jackson G.D., McIntosh A.M., Briellmann R.S., Berkovic S.F. Hippocampal sclerosis studied in identical twins. Neurology 1998, 51:78-84.
61. Jansen J.F., Lemmens E.M., Strijkers G.J., Prompers J.J., Schijns O.E., Kooi M.E., Beuls E.A., Nicolay K., Backes W.H., Hoogland G. Short- and long-term limbic abnormalities after experimental febrile seizures. Neurobiol. Dis. 2008, 32:293-301.
62. Jiang W., Duong T.M., de Lanerolle N.C. The neuropathology of hyperthermic seizures in the rat. Epilepsia 1999, 40:5-19.
63. Jung S., Jones T.D., Lugo J.N., Sheerin A.H., Miller J.W., D'Ambrosio R., Anderson A.E., Poolos N.P. Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J. Neurosci. 2007, 27:13012-13021.
64. Kanemoto K., Kawasaki J., Miyamoto T., Obayashi H., Nishimura M. Interleukin (IL)1beta, IL-1alpha, and IL-1 receptor antagonist gene polymorphisms in patients with temporal lobe epilepsy. Ann. Neurol. 2000, 47:571-574.
65. Kang J.Q., Shen W., Macdonald R.L. Why does fever trigger febrile seizures? GABAA receptor gamma2 subunit mutations associated with idiopathic generalized epilepsies have temperature-dependent trafficking deficiencies. J. Neurosci. 2006, 26:2590-2597.
66. Kang J.Q., Shen W., Macdonald R.L. 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.
67. Kapur J. Is mesial temporal sclerosis a necessary component of temporal lobe epilepsy?. Epilepsy Curr. 2006, 6:208-209.
68. Lahat E., Livne M., Barr J., Katz Y. Interleukin-1beta levels in serum and cerebrospinal fluid of children with febrile seizures. Pediatr. Neurol. 1997, 17:34-36.
69. Lee C.L., Hannay J., Hrachovy R., Rashid S., Antalffy B., Swann J.W. Spatial learning deficits without hippocampal neuronal loss in a model of early-onset epilepsy. Neuroscience 2001, 107:71-84.
70. Lemmens E.M., Lubbers T., Schijns O.E., Beuls E.A., Hoogland G. Gender differences in febrile seizure-induced proliferation and survival in the rat dentate gyrus. Epilepsia 2005, 46:1603-1612.
71. Lemmens E.M., Aendekerk B., Schijns O.E., Blokland A., Beuls E.A., Hoogland G. Long-term behavioral outcome after early-life hyperthermia-induced seizures. Epilepsy Behav. 2009, 14:309-315.
72. Lewis D.V. MRI abnormalities following febrile status epilepticus: preliminary findings from the FEBSTAT study. American Epilepsy Society Meeting 2009, IW.03 (Abstract).
73. Liu D.Z., Tian Y., Ander B.P., Xu H., Stamova B.S., Zhan X., Turner R.J., Jickling G., Sharp F.R. Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J. Cereb. Blood Flow Metab. 2010, 30:92-101.
74. Lowenstein D.H., Alldredge B.K. Status epilepticus. N. Engl. J. Med. 1998, 338:970-976.
75. Macdonald R.L., Kang J.Q., Gallagher M.J. Mutations in GABAA receptor subunits associated with genetic epilepsies. J. Physiol. 2010, 588:1861-1869.
76. Marcelin B., Chauvière L., Becker A., Migliore M., Esclapez M., Bernard C. h channel-dependent deficit of theta oscillation resonance and phase shift in temporal lobe epilepsy. Neurobiol. Dis. 2009, 33:436-447.
77. Martin M.S., Dutt K., Papale L.A., Dubé C.M., Dutton S.B., de Haan G., Shankar A., Tufik S., Meisler M.H., Baram T.Z., Goldin A.L., Escayg A. Altered function of the SCN1A voltage-gated sodium channel leads to gamma-aminobutyric acid-ergic (GABAergic) interneuron abnormalities. J. Biol. Chem. 2010, 285:9823-9834.
78. Mashimo T., Ohmori I., Ouchida M., Ohno Y., Tsurumi T., Miki T., Wakamori M., Ishihara S., Yoshida T., Takizawa A., Kato M., Hirabayashi M., Sasa M., Mori Y., Serikawa T. A missense mutation of the gene encoding voltage-dependent sodium channel (Nav1.1) confers susceptibility to febrile seizures in rats. J. Neurosci. 2010, 30:5744-5753.
79. Mathern G.W., Babb T.L., Pretorius J.K., Leite J.P. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J. Neurosci. 1995, 15:3990-4004.
80. Mathern G.W., Pretorius J.K., Babb T.L. Influence of the type of initial precipitating injury and at what age it occurs on course and outcome in patients with temporal lobe seizures. J. Neurosurg. 1995, 82:220-227.
81. Mathern G.W., Adelson P.D., Cahan L.D., Leite J.P. Hippocampal neuron damage in human epilepsy: Meyer's hypothesis revisited. Prog. Brain Res. 2002, 135:237-251.
82. Mazarati A.M., Pineda E., Shin D., Tio D., Taylor A.N., Sankar R. Comorbidity between epilepsy and depression: role of hippocampal interleukin-1beta. Neurobiol. Dis. 2010, 37:461-467.
83. McClelland S., Flynn C., Dubé C., Richichi C., Mundy J., Petrosyan R., Zha Q., Bernard C., Baram T.Z. The transcriptional repressor NRSF/REST mediates acquired HCN channelopathy in the epileptogenic process. Society for Neuroscience Meeting Neuroscience 2009, number #147.7/I9 (Abstract).
84. McClelland S., Flynn C., Dubé C., Yang J., Mundy J., Ng K., Petrosyan R., Bernard C., Baram T.Z. NRSF /REST dependent and independent gene pathways contribute to the generation of a hyperexcitable hippocampal network. Society for Neuroscience Meeting Neuroscience 2010, Session number 41 (Abstract).
85. Mikkonen M., Soininen H., Kälviänen R., Tapiola T., Ylinen A., Vapalahti M., Paljärvi L., Pitkänen A. Remodeling of neuronal circuitries in human temporal lobe epilepsy: increased expression of highly polysialylated neural cell adhesion molecule in the hippocampus and the entorhinal cortex. Ann. Neurol. 1998, 44:923-934.
86. Mueller S.G., Laxer K.D., Cashdollar N., Buckley S., Paul C., Weiner M.W. Voxel-based optimized morphometry (VBM) of gray and white matter in temporal lobe epilepsy (TLE) with and without mesial temporal sclerosis. Epilepsia 2006, 47:900-907.
87. Natsume J., Bernasconi N., Miyauchi M., Naiki M., Yokotsuka T., Sofue A., Bernasconi A. Hippocampal volumes and diffusion-weighted image findings in children with prolonged febrile seizures. Acta Neurol. Scand. Suppl. 2007, 86:25-28.
88. Nelson K.B., Ellenberg J.H. Predictors of epilepsy in children who have experienced febrile seizures. N. Engl. J. Med. 1976, 295:1029-1033.
89. Nelson K.B., Ellenberg J.H. Prognosis in children with febrile seizures. Pediatrics 1978, 61:720-727.
90. Oakley J.C., Kalume F., Yu F.H., Scheuer T., Catterall W.A. Temperature- and age-dependent seizures in a mouse model of severe myoclonic epilepsy in infancy. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3994-3999.
91. Pitkänen A., Nissinen J., Nairismägi J., Lukasiuk K., Gröhn O.H., Miettinen R., Kaupinen R. Progression of neuronal damage after status epilepticus and during spontaneous seizures in a rat model of temporal lobe epilepsy. Prog. Brain 2002, 135:67-83.
92. Powell K.L., Ng C., O'Brien T.J., Xu S.H., Williams D.A., Foote S.J., Reid C.A. Decreases in HCN mRNA expression in the hippocampus after kindling and status epilepticus in adult rats. Epilepsia 2008, 49:1686-1695.
93. Provenzale J.M., Barboriak D.P., VanLandingham K., MacFall J., Delong D., Lewis D.V. Hippocampal MRI signal hyperintensity after febrile status epilepticus is predictive of subsequent mesial temporal sclerosis. AJR Am. J. Roentgenol. 2008, 190:976-983.
94. Raol Y.S., Budreck E.C., Brooks-Kayal A.R. Epilepsy after early-life seizures can be independent of hippocampal injury. Ann. Neurol. 2003, 53:503-511.
95. Reid A.Y., Galic M.A., Teskey G.C., Pittman Q.J. Febrile seizures: current views and investigations. Can. J. Neurol. Sci. 2009, 36:679-686.
96. Salmenperä T., Könönen M., Roberts N., Vanninen R., Pitkänen A., Kälviäinen R. Hippocampal damage in newly diagnosed focal epilepsy: a prospective MRI study. Neurology 2005, 64:62-68.
97. Santoro B., Lee J.Y., Englot D.J., Gildersleeve S., Piskorowski R.A., Siegelbaum S.A., Winawer M.R., Blumenfeld H. Increased seizure severity and seizure-related death in mice lacking HCN1 channels. Epilepsia 2010, (April).
98. Sasaki K., Matsuo M., Maeda T., Zaitsu M., Hamasaki Y. Febrile seizures: characterization of double-stranded RNA-induced gene expression. Pediatr. Neurol. 2009, 41:114-118.
99. Scantlebury M.H., Ouellet P.L., Psarropoulou C., Carmant L. Freeze lesion-induced focal cortical dysplasia predisposes to atypical hyperthermic seizures in the immature rat. Epilepsia 2004, 45:592-600.
100. Scantlebury M.H., Gibbs S.A., Foadjo B., Lema P., Psarropoulou C., Carmant L. Febrile seizures in the predisposed bra a new model of temporal lobe epilepsy. Ann. Neurol. 2005, 58:41-49.
101. Schlachter K., Gruber-Sedlmayr U., Stogmann E., Lausecker M., Hotzy C., Balzar J., Schuh E., Baumgartner C., Mueller J.C., Illig T., Wichmann H.E., Lichtner P., Meitinger T., Strom T.M., Zimprich A., Zimprich F. A splice site variant in the sodium channel gene SCN1A confers risk of febrile seizures. Neurology 2009, 72:974-978.
102. Scott R.C., Gadian D.G., King M.D., Chong W.K., Cox T.C., Neville B.G., Connelly A. Magnetic resonance imaging findings within 5days of status epilepticus in childhood. Brain 2002, 125:1951-1959.
103. Scott R.C., King M.D., Gadian D.G., Neville B.G., Connelly A. Hippocampal abnormalities after prolonged febrile convulsion: a longitudinal MRI study. Brain 2003, 126:2551-2557.
104. Sharp F.R., Lit L., Xu H., Apperson M., Walker W., Wong B., Gilbert D.L., Hershey A., Glauser T.A. Genomics of brain and blood: progress and pitfalls. Epilepsia 2006, 47:1603-1607.
105. Shinnar S. Febrile seizures and mesial temporal sclerosis. Epilepsy Curr. 2003, 3:115-118.
106. Shinnar S., Berg A.T., Moshe S.L., Shinnar R. How long do new-onset seizures in children last?. Ann. Neurol. 2001, 49:659-664.
107. Shinnar S., Hesdorffer D.C., Nordli D.R., Pellock J.M., O'Dell C., Lewis D.V., Frank L.M., Moshé S.L., Epstein L.G., Marmarou A., Bagiella E. Phenomenology of prolonged febrile seizures: results of the FEBSTAT study. Neurology 2008, 71:170-176. FEBSTAT Study Team.
108. Sloviter R.S. The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann. Neurol. 1994, 35:640-654.
109. Spampanato J., Escayg A., Meisler M.H., Goldin A.L. Functional effects of two voltage-gated sodium channel mutations that cause generalized epilepsy with febrile seizures plus type 2. J. Neurosci. 2001, 21:7481-7490.
110. Spampanato J., Kearney J.A., de Haan G., McEwen D.P., Escayg A., Aradi I., MacDonald B.T., Levin S.I., Soltesz I., Benna P., Montalenti E., Isom L.L., Goldin A.L., Meisler M.H. A novel epilepsy mutation in the sodium channel SCN1A identifies a cytoplasmic domain for beta subunit interaction. J. Neurosci. 2004, 24:10022-10034.
111. Spreafico R., Tassi L., Colombo N., Bramerio M., Galli C., Garbelli R., Ferrario A., Lo Russo G., Munari C. Inhibitory circuits in human dysplastic tissue. Epilepsia 2000, 41(Suppl. 6):S168-173.
112. Stafstrom C.E. The incidence and prevalence of febrile seizures. Febrile Seizures 2002, 1-25. Academic Press, San Diego. T.Z. Baram, S. Shinnar (Eds.).
113. Stores G. When does an EEG contribute to the management of febrile seizures?. Arch. Dis. Child. 1991, 66:554-557.
114. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber reorganization in the epileptic human temporal lobe. Ann. Neurol. 1989, 26:321-330.
115. Tapia-Ramirez J., Eggen B.J., Peral-Rubio M.J., Toledo-Aral J.J., Mandel G. A single zinc finger motif in the silencing factor REST represses the neural-specific type II sodium channel promoter. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1177-1182.
116. Theodore W.H., Bhatia S., Hatta J., Fazilat S., DeCarli C., Bookheimer S.Y., Gaillard W.D. Hippocampal atrophy, epilepsy duration, and febrile seizures in patients with partial seizures. Neurology 1999, 52:132-136.
117. Thomas E.A, Hawkins R.J., Richards K.L., Xu R., Gazina E.V., Petrou S. Heat opens axon initial segment sodium channels: a febrile seizure mechanism?. Ann. Neurol. 2009, 66:219-226.
118. Tomoum H.Y., Badawy N.M., Mostafa A.A., Harb M.Y. Plasma interleukin-1beta levels in children with febrile seizures. J. Child Neurol. 2007, 22:689-692.
119. Toth Z., Yan X.X., Haftoglou S., Ribak C.E., Baram T.Z. Seizure-induced neuronal injury: vulnerability to febrile seizures in an immature rat model. J. Neurosci. 1998, 18:4285-4294.
120. VanLandingham K.E., Heinz E.R., Cavazos J.E., Lewis D.V. Magnetic resonance imaging evidence of hippocampal injury after prolonged focal febrile convulsions. Ann. Neurol. 1998, 43:413-426.
121. Verity C.M., Butler N.R., Golding J. Febrile convulsions in a national cohort followed up from birth. II-medical history and intellectual ability at 5years of age. Br. Med. J. 1985, 290:1311-1315.
122. Verity C.M., Greenwood R., Golding J. Long-term intellectual and behavioral outcomes of children with febrile convulsions. N. Engl. J. Med. 1998, 338:1723-1728.
123. Vezzani A., Baram T.Z. New roles for interleukin-1 beta in the mechanisms of epilepsy. Epilepsy Curr. 2007, 7:45-50.
124. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2010.
125. Vincent A., Irani S.R., Lang B. The growing recognition of immunotherapy-responsive seizure disorders with autoantibodies to specific neuronal proteins. Curr. Opin. Neurol. 2010, 23:144-150.
126. Virta M., Hurme M., Helminen M. Increased plasma levels of pro- and anti-inflammatory cytokines in patients with febrile seizures. Epilepsia 2002, 43:920-923.
127. Virta M., Hurme M., Helminen M. Increased frequency of interleukin-1beta (-511) allele 2 in febrile seizures. Pediatr. Neurol. 2002, 26:192-195.
128. Wallace R.H., Wang D.W., Singh R., Scheffer I.E., George A.L., Phillips H.A., Saar K., Reis A., Johnson E.W., Sutherland G.R., Berkovic S.F., Mulley J.C. Febrile seizures and generalized epilepsy associated with a mutation in the Na+-channel beta1 subunit gene SCN1B. Nat. Genet. 1998, 19:366-370.
129. Xu R., Thomas E.A., Gazina E.V., Richards K.L., Quick M., Wallace R.H., Harkin L.A., Heron S.E., Berkovic S.F., Scheffer I.E., Mulley J.C., Petrou S. Generalized epilepsy with febrile seizures plus-associated sodium channel beta1 subunit mutations severely reduce beta subunit-mediated modulation of sodium channel function. Neuroscience 2007, 148:164-174.
130. Zerr D.M., Meier A.S., Selke S.S., Frenkel L.M., Huang M.L., Wald A., Rhoads M.P., Nguy L., Bornemann R., Morrow R.A., Corey L. A population-based study of primary human herpesvirus 6 infection. N. Engl. J. Med. 2005, 352:768-776.
131. Zhang X., Cui S.S., Wallace A.E., Hannesson D.K., Schmued L.C., Saucier D.M., Honer W.G., Corcoran M.E. Relations between brain pathology and temporal lobe epilepsy. J. Neurosci. 2002, 22:6052-6061.