Seizures and epilepsy in herpes simplex virus encephalitis: Current concepts and future directions of pathogenesis and management

Journal of Neurology

Volumn 259, Issue 10, 2012, Pages 2019-2030

  Sellner, Johann ^a,b,c   Trinka, Eugen ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c Krankenhaus Hietzing mit Neurologischem Zentrum Rosenhugel   (Austria)

Author keywords

Epilepsy; Herpes encephalitis; Intractable; Seizures; Surgery

Indexed keywords

ACICLOVIR; ANTICONVULSIVE AGENT; ANTIVIRUS AGENT; BENZODIAZEPINE; CARBAMAZEPINE; CORTICOSTEROID; CYTOKINE; ETIRACETAM; GABAPENTIN; HARKOSERIDE; LAMOTRIGINE; OXCARBAZEPINE; PHENOBARBITAL; PHENYTOIN; TOPIRAMATE; VALACICLOVIR; VALPROIC ACID; ZONISAMIDE;

ANTICONVULSANT THERAPY; AUTOIMMUNE DISEASE; CLINICAL FEATURE; DECOMPRESSIVE CRANIECTOMY; DRUG CONTRAINDICATION; ELECTROENCEPHALOGRAM; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; FEVER; HEMISPHERECTOMY; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS; HUMAN; IMMUNE RESPONSE; LOW DRUG DOSE; MOLECULAR PATHOLOGY; NERVE INJURY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PATHOPHYSIOLOGY; PREGNANCY; PRIORITY JOURNAL; PROGNOSIS; RECURRENT DISEASE; REVIEW; SEIZURE; STEROID THERAPY; TREATMENT OUTCOME; TREATMENT RESPONSE;

ENCEPHALITIS, HERPES SIMPLEX; EPILEPSY; HUMANS; SEIZURES;

EID: 84867332245     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-012-6494-6     Document Type: Review

References (108)

1. Annegers JF, Hauser WA, Beghi E, Nicolosi A, Kurland LT (1988) The risk of unprovoked seizures after encephalitis and meningitis. Neurology 38:1407-1410
2. Aravalli RN, Hu S, Rowen TN, Palmquist JM, Lokensgard JR (2005) Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J Immunol 175:4189-4193
3. Aurelius E, Andersson B, Forsgren M, Skoldenberg B, Strannegard O (1994) Cytokines and other markers of intrathecal immune response in patients with herpes simplex encephalitis. J Infect Dis 170:678-681
4. Baek MY, Kim YM, Lee YJ, Nam SO (2010) Risk factors for epilepsy after central nervous system infection in children. Korean Child Neurol Soc 18:33-39
5. Baringer JR (2008) Herpes simplex infections of the nervous system. Neurol Clin 26:657-674, viii
6. Baringer JR, Pisani P (1994) Herpes simplex virus genomes in human nervous system tissue analyzed by polymerase chain reaction. Ann Neurol 36:823-829
7. Baulac S, Gourfinkel-An I, Nabbout R, Huberfeld G, Serratosa J, Leguern E, Baulac M (2004) Fever, genes, and epilepsy. Lancet Neurol 3:421-430
8. Beers DR, Henkel JS, Schaefer DC, Rose JW, Stroop WG (1993) Neuropathology of herpes simplex virus encephalitis in a rat seizure model. J Neuropathol Exp Neurol 52:241-252
9. Cagnin A, Myers R, Gunn RN, Lawrence AD, Stevens T, Kreutzberg GW, Jones T, Banati RB (2001) In vivo visualization of activated glia by [11C] (R)-PK11195-PET following herpes encephalitis reveals projected neuronal damage beyond the primary focal lesion. Brain 124:2014-2027
10. Chen SF, Huang CC, Wu HM, Chen SH, Liang YC, Hsu KS (2004) Seizure, neuron loss, and mossy fiber sprouting in herpes simplex virus type 1-infected organotypic hippocampal cultures. Epilepsia 45:322-332
11. Chen YJ, Fang PC, Chow JC (2006) Clinical characteristics and prognostic factors of postencephalitic epilepsy in children. J Child Neurol 21:1047-1051
12. Conrady CD, Drevets DA, Carr DJ (2010) Herpes simplex type I (HSV-1) infection of the nervous system: is an immune response a good thing? J Neuroimmunol 220:1-9
13. De Tiege X, De Laet C, Mazoin N, Christophe C, Mewasingh LD, Wetzburger C, Dan B (2005) Postinfectious immune-mediated encephalitis after pediatric herpes simplex encephalitis. Brain Dev 27:304-307
14. De Tiege X, Rozenberg F, Burlot K, Gaudelus J, Ponsot G, Heron B (2006) Herpes simplex encephalitis: diagnostic problems and late relapse. Dev Med Child Neurol 48:60-63
15. De Tiege X, Rozenberg F, Des Portes V, Lobut JB, Lebon P, Ponsot G, Heron B (2003) Herpes simplex encephalitis relapses in children: differentiation of two neurologic entities. Neurology 61:241-243
16. De Tiege X, Rozenberg F, Heron B (2008) The spectrum of herpes simplex encephalitis in children. Eur J Paediatr Neurol 12:72-81
17. Donaire A, Carreno M, Agudo R, Delgado P, Bargallo N, Setoain X, Boget T, Raspall T, Falip M, Rumia J, Pintor L, Maestro I (2007) Presurgical evaluation in refractory epilepsy secondary to meningitis or encephalitis: bilateral memory deficits often preclude surgery. Epileptic Disord 9:127-133
18. Elbers JM, Bitnun A, Richardson SE, Ford-Jones EL, Tellier R, Wald RM, Petric M, Kolski H, Heurter H, MacGregor D (2007) A 12-year prospective study of childhood herpes simplex encephalitis: is there a broader spectrum of disease? Pediatrics 119:e399-e407
19. Engel J Jr, Wiebe S, French J, Sperling M, Williamson P, Spencer D, Gumnit R, Zahn C, Westbrook E, Enos B (2003) Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the Quality Standards Subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology 60:538-547
20. Erba C, Visoná R, Zeroli C, Pravettoni G, Cocca G, Quirino T (2006) Herpes simplex encephalitis relapse: a case report. Case Rep Clin Pract Rev 7:27-29
21. Fabene PF, Bramanti P, Constantin G (2010) The emerging role for chemokines in epilepsy. J Neuroimmunol 224:22-27
22. Fowler A, Stodberg T, Eriksson M, Wickstrom R (2010) Longterm outcomes of acute encephalitis in childhood. Pediatrics 126:e828-e835
23. Free SL, Li LM, Fish DR, Shorvon SD, Stevens JM (1996) Bilateral hippocampal volume loss in patients with a history of encephalitis or meningitis. Epilepsia 37:400-405
24. Friedman A, Dingledine R (2010) Molecular cascades that mediate the influence of inflammation on epilepsy. Epilepsia 52(Suppl 3):33-39
25. Gilden DH, Mahalingam R, Cohrs RJ, Tyler KL (2007) Herpesvirus infections of the nervous system. Nat Clin Pract Neurol 3:82-94
26. Gong T, Bingaman W, Danziger-Isakov L, Tuxhorn I, Goldfarb J (2010) Herpes simplex virus reactivation after subtotal hemispherectomy in a pediatric patient. Pediatr Infect Dis J 29:1148-1150
27. Granerod J, Ambrose HE, Davies NW, Clewley JP, Walsh AL, Morgan D, Cunningham R, Zuckerman M, Mutton KJ, Solomon T, Ward KN, Lunn MP, Irani SR, Vincent A, Brown DW, Crowcroft NS (2011) Causes of encephalitis and differences in their clinical presentations in England: a multicentre, population-based prospective study. Lancet Infect Dis 10:835-844
28. Hjalmarsson A, Blomqvist P, Skoldenberg B (2007) Herpes simplex encephalitis in Sweden, 1990-2001: incidence, morbidity, and mortality. Clin Infect Dis 45:875-880
29. Höfler J, Unterberger I, Dobesberger J, Kuchukhidze G, Walser G, Trinka E (2011) Intravenous lacosamide in status epilepticus and seizure clusters. Epilepsia 52:148-152
30. Holtkamp M, Othman J, Buchheim K, Meierkord H (2005) Predictors and prognosis of refractory status epilepticus treated in a neurological intensive care unit. J Neurol Neurosurg Psychiatry 76:534-539
31. Hsieh WB, Chiu NC, Hu KC, Ho CS, Huang FY (2007) Outcome of herpes simplex encephalitis in children. J Microbiol Immunol Infect 40:34-38
32. Ichiyama T, Shoji H, Takahashi Y, Matsushige T, Kajimoto M, Inuzuka T, Furukawa S (2008) Cerebrospinal fluid levels of cytokines in non-herpetic acute limbic encephalitis: comparison with herpes simplex encephalitis. Cytokine 44:149-153
33. Ito Y, Kimura H, Yabuta Y, Ando Y, Murakami T, Shiomi M, Morishima T (2000) Exacerbation of herpes simplex encephalitis after successful treatment with acyclovir. Clin Infect Dis 30:185-187
34. Joos AA, Ziyeh S, Rauer S, Keller E, Huzly D, Lucking CH (2003) Postinfectious autoimmune-mediated encephalitis eight months after herpes simplex encephalitis. Eur Neurol 50:54-56
35. Kalita J, Nair PP, Misra UK (2008) Status epilepticus in encephalitis: a study of clinical findings, magnetic resonance imaging, and response to antiepileptic drugs. J Neurovirol 14:412-417
36. Kamei S, Sekizawa T, Shiota H, Mizutani T, Itoyama Y, Takasu T, Morishima T, Hirayanagi K (2005) Evaluation of combination therapy using aciclovir and corticosteroid in adult patients with herpes simplex virus encephalitis. J Neurol Neurosurg Psychiatry 76:1544-1549
37. Kamei S, Taira N, Ishihara M, Sekizawa T, Morita A, Miki K, Shiota H, Kanno A, Suzuki Y, Mizutani T, Itoyama Y, Morishima T, Hirayanagi K (2009) Prognostic value of cerebrospinal fluid cytokine changes in herpes simplex virus encephalitis. Cytokine 46:187-193
38. Kimura H, Aso K, Kuzushima K, Hanada N, Shibata M, Morishima T (1992) Relapse of herpes simplex encephalitis in children. Pediatrics 89:891-894
39. Kirkman NJ, Libbey JE, Wilcox KS, White HS, Fujinami RS (2010) Innate but not adaptive immune responses contribute to behavioral seizures following viral infection. Epilepsia 51:454-464
40. Knickelbein JE, Khanna KM, Yee MB, Baty CJ, Kinchington PR, Hendricks RL (2008) Noncytotoxic lytic granule-mediated CD8? T cell inhibition of HSV-1 reactivation from neuronal latency. Science 322:268-271
41. Kumar G, Kalita J, Misra UK (2009) Raised intracranial pressure in acute viral encephalitis. Clin Neurol Neurosurg 111:399-406
42. Lahat E, Barr J, Barkai G, Paret G, Brand N, Barzilai A (1999) Long term neurological outcome of herpes encephalitis. Arch Dis Child 80:69-71
43. Lancman ME, Morris HH 3rd (1996) Epilepsy after central nervous system infection: clinical characteristics and outcome after epilepsy surgery. Epilepsy Res 25:285-290
44. Lee JH, Lee BI, Park SC, Kim WJ, Kim JY, Park SA, Huh K (1997) Experiences of epilepsy surgery in intractable seizures with past history of CNS infection. Yonsei Med J 38:73-78
45. Lee JH, Nam DH, Oh SY, Shin BS, Seo MW, Jeong SK, Lee JY (2012) Nonconvulsive Status Epilepticus Presenting as Epileptic Nystagmus in a Patient With Herpes Encephalitis. J Neuroophthalmol: in press
46. Lee WT, Yu TW, Chang WC, Shau WY (2007) Risk factors for postencephalitic epilepsy in children: a hospital-based study in Taiwan. Eur J Paediatr Neurol 11:302-309
47. Lellouch-Tubiana A, Fohlen M, Robain O, Rozenberg F (2000) Immunocytochemical characterization of long-term persistent immune activation in human brain after herpes simplex encephalitis. Neuropathol Appl Neurobiol 26:285-294
48. Leung AK, Robson WL (2007) Febrile seizures. J Pediatr Health Care 21:250-255
49. Lokensgard JR, Hu S, Sheng W, van Oijen M, Cox D, Cheeran MC, Peterson PK (2001) Robust expression of TNF-alpha, IL-1beta, RANTES, and IP-10 by human microglial cells during nonproductive infection with herpes simplex virus. J Neurovirol 7:208-219
50. Lundberg P, Ramakrishna C, Brown J, Tyszka JM, Hamamura M, Hinton DR, Kovats S, Nalcioglu O, Weinberg K, Openshaw H, Cantin EM (2008) The immune response to herpes simplex virus type 1 infection in susceptible mice is a major cause of central nervous system pathology resulting in fatal encephalitis. J Virol 82:7078-7088
51. Maia R, Gouveia C, Moreira A, Casanova JL, Sancho-Shimizu V, Brito MJ (2011) Early ''relapsé' after herpetic encephalitis: extensive white matter lesions in an infant with interferon production deficit. J Child Neurol 26:369-372
52. Mailles A, Stahl JP (2009) Infectious encephalitis in France in 2007: a national prospective study. Clin Infect Dis 49:1838-1847
53. Malipiero U, Heuss C, Schlapbach R, Tschopp J, Gerber U, Fontana A (1999) Involvement of the N-methyl-D-aspartate receptor in neuronal cell death induced by cytotoxic T cellderived secretory granules. Eur J Immunol 29:3053-3062
54. Mandyla H, Anagnostakis D, Koutsovitis P, Siahanidou T, Youroukos S (2001) Late recurrence of herpes simplex virus meningoencephalitis in two infants. Eur J Pediatr 160:732-735
55. Marks DA, Kim J, Spencer DD, Spencer SS (1992) Characteristics of intractable seizures following meningitis and encephalitis. Neurology 42:1513-1518
56. Marques CP, Cheeran MC, Palmquist JM, Hu S, Urban SL, Lokensgard JR (2008) Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J Immunol 181:6417-6426
57. Martinez-Torres F, Menon S, Pritsch M, Victor N, Jenetzky E, Jensen K, Schielke E, Schmutzhard E, de Gans J, Chung CH, Luntz S, Hacke W, Meyding-Lamade U (2008) Protocol for German trial of Acyclovir and corticosteroids in Herpes-simplex-virus-encephalitis (GACHE): a multicenter, multinational, randomized, double-blind, placebo-controlled German, Austrian and Dutch trial [ISRCTN45122933]. BMC Neurol 8:40
58. Mayer SA, Claassen J, Lokin J, Mendelsohn F, Dennis LJ, Fitzsimmons BF (2002) Refractory status epilepticus: frequency, risk factors, and impact on outcome. Arch Neurol 59:205-210
59. McGrath N, Anderson NE, Croxson MC, Powell KF (1997) Herpes simplex encephalitis treated with acyclovir: diagnosis and long term outcome. J Neurol Neurosurg Psychiatry 63:321-326
60. Mekan SF, Wasay M, Khelaeni B, Saeed Z, Hassan A, Sheerani M (2005) Herpes simplex encephalitis: analysis of 68 cases from a tertiary care hospital in Karachi, Pakistan. J Pak Med Assoc 55:146-148
61. Misra UK, Kalita J (1998) Neurophysiological studies in herpes simplex encephalitis. Electromyogr Clin Neurophysiol 38:177-182
62. Misra UK, Kalita J (2009) Seizures in encephalitis: predictors and outcome. Seizure 18:583-587
63. Misra UK, Kalita J, Nair PP (2008) Status epilepticus in central nervous system infections: an experience from a developing country. Am J Med 121:618-623
64. Misra UK, Tan CT, Kalita J (2008) Viral encephalitis and epilepsy. Epilepsia 49(Suppl 6):13-18
65. Nahmias AJ, Whitley RJ, Visintine AN, Takei Y, Alford CA Jr (1982) Herpes simplex virus encephalitis: laboratory evaluations and their diagnostic significance. J Infect Dis 145:829-836
66. O'Brien TJ, Moses H, Cambier D, Cascino GD (2002) Age of meningitis or encephalitis is independently predictive of outcome from anterior temporal lobectomy. Neurology 58:104-109
67. Parmeggiani A, Riva R, Posar A, Rossi PG (1995) Possible interaction between acyclovir and antiepileptic treatment. Ther Drug Monit 17:312-315
68. Perucca E, Tomson T (2011) The pharmacological treatment of epilepsy in adults. Lancet Neurol 10:446-456
69. Radermecker J (1949) Aspects électroencephalographiques dans trois cas d'encéphalite subaigué. Acta Neurol Belg 49:222-232
70. Ravizza T, Gagliardi B, Noe F, Boer K, Aronica E, Vezzani A (2008) Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 29:142-160
71. Reid AY, Galic MA, Teskey GC, Pittman QJ (2009) Febrile seizures: current views and investigations. Can J Neurol Sci 36:679-686
72. Rijkers K, Majoie HJ, Hoogland G, Kenis G, De Baets M, Vles JS (2009) The role of interleukin-1 in seizures and epilepsy: a critical review. Exp Neurol 216:258-271
73. Rozenberg F, Deback C, Agut H (2011) Herpes simplex encephalitis: from virus to therapy. Infect Disord Drug Targets 11:235-250
74. Schlitt M, Bucher AP, Stroop WG, Pindak F, Bastian FO, Jennings RA, Lakeman AD, Whitley RJ (1988) Neurovirulence in an experimental focal herpes encephalitis: relationship to observed seizures. Brain Res 440:293-298
75. Sellner J, Buonomano R, Nedeltchev K, Findling O, Schroth G, Surbek DV, Leib SL (2009) A case of maternal herpes simplex virus encephalitis during late pregnancy. Nat Clin Pract Neurol 5:51-56
76. Sellner J, Dvorak F, Zhou Y, Haas J, Kehm R, Wildemann B, Meyding-Lamade U (2005) Acute and long-term alteration of chemokine mRNA expression after anti-viral and antiinflammatory treatment in herpes simplex virus encephalitis. Neurosci Lett 374:197-202
77. Sellner J, Simon F, Meyding-Lamade U, Leib SL (2006) Herpes-simplex virus encephalitis is characterized by an early MMP-9 increase and collagen type IV degradation. Brain Res 1125:155-162
78. Sergerie Y, Rivest S, Boivin G (2007) Tumor necrosis factoralpha and interleukin-1 beta play a critical role in the resistance against lethal herpes simplex virus encephalitis. J Infect Dis 196:853-860
79. Shimeld C, Efstathiou S, Hill T (2001) Tracking the spread of a lacZ-tagged herpes simplex virus type 1 between the eye and the nervous system of the mouse: comparison of primary and recurrent infection. J Virol 75:5252-5262
80. Shorvon S (2010) Handbook of Epilepsy Treatment. Wiley-Blackwell, Oxford
81. Shorvon S, Baulac M, Cross H, Trinka E, Walker M (2008) The drug treatment of status epilepticus in Europe: consensus document from a workshop at the first London Colloquium on Status Epilepticus. Epilepsia 49:1277-1285
82. Skoldenberg B, Aurelius E, Hjalmarsson A, Sabri F, Forsgren M, Andersson B, Linde A, Strannegard O, Studahl M, Hagberg L, Rosengren L (2006) Incidence and pathogenesis of clinical relapse after herpes simplex encephalitis in adults. J Neurol 253:163-170
83. Smith JB, Westmoreland BF, Reagan TJ, Sandok BA (1975) A distinctive clinical EEG profile in herpes simplex encephalitis. Mayo Clin Proc 50:469-474
84. Smith MG, Lennette EH, Reames HR (1941) Isolation of the virus of herpes simplex and the demonstration of intranuclear inclusions in a case of acute encephalitis. Am J Pathol 17(55-68):51
85. Solbrig MV, Adrian R, Chang DY, Perng GC (2006) Viral risk factor for seizures: pathobiology of dynorphin in herpes simplex viral (HSV-1) seizures in an animal model. Neurobiol Dis 23:612-620
86. Solomon T, Hart IJ, Beeching NJ (2007) Viral encephalitis: a clinician's guide. Pract Neurol 7:288-305
87. Spiegel R, Miron D, Yodko H, Lumelsky D, Habib A, Horovitz Y (2008) Late relapse of herpes simplex virus encephalitis in a child due to reactivation of latent virus: clinicopathological report and review. J Child Neurol 23:344-348
88. Stahl JP, Mailles A, De Broucker T (2011) Herpes simplex encephalitis and management of acyclovir in encephalitis patients in France. Epidemiol Infect:1-10
89. Steiner I, Budka H, Chaudhuri A, Koskiniemi M, Sainio K, Salonen O, Kennedy PG (2010) Viral meningoencephalitis: a review of diagnostic methods and guidelines for management. Eur J Neurol 17:999-e957
90. Studahl M, Sköldenberg B (2006) Herpes simplex encephalitis and other neurological syndromes caused by herpes simplex virus-1. In: Studahl M, Cinque P, Bergström T (eds) Herpes simplex viruses. Taylor & Francis, New York, pp 275-316
91. Trinka E (2004) Presurgical evaluation in patients with inflammatory lesions: meningitis, encephalitis, and Rasmussen's syndrome. In: Rosenow F, Lüders HO (eds) Handbook of Clinical Neurophysiology. Elsevier, Amsterdam, pp 423-440
92. Trinka E (2011) What is the evidence to use new intravenous AEDs in status epilepticus? Epilepsia 52:35-38
93. Trinka E (2009) What is the relative value of the standard anticonvulsants: phenytoin and fosphenytoin, phenobarbital, valproate, and levetiracetam? Epilepsia 50(Suppl 12):40-43
94. Trinka E, Dubeau F, Andermann F, Bastos A, Hui A, Li LM, Kohler S, Olivier A (2000) Clinical findings, imaging characteristics and outcome in catastrophic post-encephalitic epilepsy. Epileptic Disord 2:153-162
95. Trinka E, Dubeau F, Andermann F, Hui A, Bastos A, Li LM, Kohler S, Olivier A (2000) Successful epilepsy surgery in catastrophic postencephalitic epilepsy. Neurology 54:2170-2173
96. Tyler KL (2004) Herpes simplex virus infections of the central nervous system: encephalitis and meningitis, including Mollaret's. Herpes 11(Suppl 2):57A-64A
97. Valencia I, Miles DK, Melvin J, Khurana D, Kothare S, Hardison H, Legido A (2004) Relapse of herpes encephalitis after acyclovir therapy: report of two new cases and review of the literature. Neuropediatrics 35:371-376
98. van Jaarsveld MF, Walubo A, du Plessis JB (2007) Interaction between valproic acid and acyclovir after intravenous and oral administration in a rabbit model. Basic Clin Pharmacol Toxicol 101:434-440
99. Vezzani A, Aronica E, Mazarati A, Pittman QJ (2011) Epilepsy and brain inflammation. Exp Neurol (in press). PMID:21985866
100. Vezzani A, Moneta D, Conti M, Richichi C, Ravizza T, De Luigi A, De Simoni MG, Sperk G, Andell-Jonsson S, Lundkvist J, Iverfeldt K, Bartfai T (2000) Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc Natl Acad Sci USA 97:11534-11539
101. Wasay M, Mekan SF, Khelaeni B, Saeed Z, Hassan A, Cheema Z, Bakshi R (2005) Extra temporal involvement in herpes simplex encephalitis. Eur J Neurol 12:475-479
102. Whitley RJ (2006) Herpes simplex encephalitis: adolescents and adults. Antiviral Res 71:141-148
103. Whitley RJ, Alford CA, Hirsch MS, Schooley RT, Luby JP, Aoki FY, Hanley D, Nahmias AJ, Soong SJ (1986) Vidarabine versus acyclovir therapy in herpes simplex encephalitis. N Engl J Med 314:144-149
104. Whitley RJ, Soong SJ, Linneman C Jr, Liu C, Pazin G, Alford CA (1982) Herpes simplex encephalitis. Clinical Assessment. JAMA 247:317-320
105. Wu HM, Huang CC, Chen SH, Liang YC, Tsai JJ, Hsieh CL, Hsu KS (2003) Herpes simplex virus type 1 inoculation enhances hippocampal excitability and seizure susceptibility in mice. Eur J Neurosci 18:3294-3304
106. Xu F, Sternberg MR, Kottiri BJ, McQuillan GM, Lee FK, Nahmias AJ, Berman SM, Markowitz LE (2006) Trends in herpes simplex virus type 1 and type 2 seroprevalence in the United States. JAMA 296:964-973
107. Yoshioka M, Kuroki S, Mizue H (1989) Clinical and electroencephalographic studies of postencephalitic epilepsy. Acta Paediatr Jpn 31:480-483
108. Zattoni M, Mura ML, Deprez F, Schwendener RA, Engelhardt B, Frei K, Fritschy JM (2011) Brain infiltration of leukocytes contributes to the pathophysiology of temporal lobe epilepsy. J Neurosci 31:4037-4050