Recent advances in pathophysiology studies and treatment of epilepsy in neurocutaneous disorders

Sadowski, Krzysztof; Jóźwiak, Sergiusz

doi:10.21307/joepi-2015-0017

Abstract

Introduction

Epilepsy that is associated with neurocutaneous disorders seriously deteriorates quality of life and cognitive outcome of affected children. Recent advances in epilepsy pathophysiology raise hopes for better treatment results in this difficult group of patients.

Aim

The aim of this review is to present recent treatment recommendations as well as current research progress in the most frequent neurocutaneous disorders.

Material and methods

We analyzed PubMed database to select the most prominent and recent (up to 2014 year) publications on the treatment and mechanisms of epilepsy in selected neurocutaneous disorders. We aimed to emphasize evidence-based medicine recommendations as well as basic experimental studies dealing with molecular mechanisms of epileptogenesis.

Discussion and conclusions

Recent advances in disease-modifying treatment options such as mTOR inhibitors in patients with tuberous sclerosis complex open up new perspectives for neurologists. Traditional resective surgery has still a major role as a treatment of choice in carefully selected cases.

References

Alkonyi B., Chugani HT., Juhasz C.:Transient focal cortical increase of interictal glucose metabolism in Sturge-Weber syndrome: implications for epileptogenesis. Epilepsia, 2011, 52: 1265–1272.10.1111/j.1528-1167.2011.03066.x
Search in Google Scholar Back to article
Arun D., Gutmann D.H.:Recent advances in neurofibromatosis 1. Curr. Opin. Neurol., 2004, 17: 101–105.10.1097/00019052-200404000-00004
Search in Google Scholar Back to article
Arzimanoglou A., Aicardi J.:The epilepsy of Sturge-Weber syndrome: clinical features and treatment in 23 patients. Acta Neurol. Scand., Suppl., 1992, 140: 18–22.10.1111/j.1600-0404.1992.tb04465.x
Search in Google Scholar Back to article
Barba C., Jaques T., Kahane P., Polster T., Isnard J., Leijten F.S. et al.:Epilepsy surgery in Neurofibromatosis Type 1. Epilepsy Res., 2013, 105: 384–395.10.1016/j.eplepsyres.2013.02.021
Search in Google Scholar Back to article
Bebin E.M., Gomez M.R.:Prognosis in Sturge-Weber disease: comparison of unihemisspheric and bihemispheric involvement. J. Child. Neurol., 1992, 3: 181–184.10.1177/088307388800300306
Search in Google Scholar Back to article
Benedikt R.A., Brown D.C., Walker R., Ghaed V.N., Mitchell M., Geyer C.A.:Sturge-Weber syndrome: cranial MR imaging with Gd-DTPA. Am. J. Neurorad., 1993, 14: 1409–1415. Chugani H.T., Luat A.F., Kumar A., Govindan R., Pawlik K., Asano E.:α-[11C]-Methyl-L-tryptophan-PET in 191 patients with tuberous sclerosis complex. Neurology, 2013, 81: 674–680. Chu-Shore C.J., Major P., Camposano S., Muzykewicz D., Thiele E.A.:The natural history of epilepsy in tuberous sclerosis complex. Epilepsia, 2010, 51: 1236–1241.
Search in Google Scholar Back to article
Comi A.M.:Update on Sturge-Weber syndrome: diagnosis, treatment, quantitative measures, and controversies. Lymphat. Res. Biol., 2007, 5: 257–264.10.1089/lrb.2007.1016
Search in Google Scholar Back to article
Comi A.M., Bellamkonda S., Ferenc L.M., Cohen B.A., Germain-Lee E.L.:Central hypothyroidism and Sturge-Weber syndrome. Pediatr. Neurol., 2008, 39: 58–62.10.1016/j.pediatrneurol.2008.03.018
Search in Google Scholar Back to article
Crumrine P.K.:Mamagement of seizures in Lennox-Gastaut syndrome. Paediatr. Drugs., 2011, 13: 107–118.10.2165/11536940-000000000-00000
Search in Google Scholar Back to article
Curatolo P., Bombardieri R., Jóźwiak S.:Tuberous sclerosis. Lancet, 2008, 372: 657–668.10.1016/S0140-6736(08)61279-9
Search in Google Scholar Back to article
Curatolo P., Jóźwiak S., Nabbout R.:Management of epilepsy associated with tuberous sclerosis complex (TSC): Clinical recommendations. Eur. J. Paediatr. Neurol., 2012, 16: 582–586.10.1016/j.ejpn.2012.05.00422695035
Search in Google Scholar Back to article
DiFrancesco J.C., Sestini R., Cossu F., Bolognesi M., Sala E., Mariani S. et al.:Novel neurofibromatosis type 2 mutation presenting with status epilepticus. Epileptic Disord., 2014, 16: 132–137.10.1684/epd.2014.0647
Search in Google Scholar Back to article
Domańska-Pakieła D., Kaczorowska M., Jurkiewicz E., Kotulska K., Dunin-Wąsowicz D., Jóźwiak S.:EEG abnormalities preceding the epilepsy onset in tuberous sclerosis complex patients-A prospective study of 5 patients. Eur. J. Paediatr. Neurology, 2014, 18: 458–468.10.1016/j.ejpn.2013.12.006
Search in Google Scholar Back to article
Kossoff E.H., Borsage J.L., Comi A.L.:A pilot study of the modified Atkins diet for Sturge-Weber syndrome. Epilepsy Res., 2010, 92: 240–243.10.1016/j.eplepsyres.2010.09.008
Search in Google Scholar Back to article
Elliot R.E., Carlson C., Kalhorn S.P., Moshel Y.A., Weiner H.L., Devinsky O. et al.:Refractory epilepsy in tuberous sclerosis: vagus nerve stimulation with or without subsequent resective surgery. Epilepsy Behav., 2009, 16: 454–460.10.1016/j.yebeh.2009.08.018
Search in Google Scholar Back to article
Fallah A., Guyatt G.H., Snead O.C., Ebrahim S., Ibrahim G.M., Mansouri A. et al.:Predictors of seizure outcomes in children with tuberous sclerosis complex and intractable epilepsy undergoing resective epilepsy surgery: an individual participant data meta-analysis. PLoS One., 2013, 8: e53565.10.1371/journal.pone.0053565
Search in Google Scholar Back to article
Franz D.N., Belousova E., Sparagana S., Bebin E.M., Frost M., Kuperman R. et al.:Efficacy and safety of everolimus for subependymal giant cell astrocytomas associated with tuberous sclerosis complex (EXIST-1): a multicentre, randomised, placebo-controlled phase 3 trial. Lancet, 2013, 381: 125–132.10.1016/S0140-6736(12)61134-9
Search in Google Scholar Back to article
Friedman D., Bogner M., Parker-Menzer K., Devinsky O.:Vigabatrin for partial-onset seizure treatment in patients with tuberous sclerosis complex. Epilepsy Behav., 2013, 27: 118–120. Guerreiro M.M., Andermann F., Andermann E., Palmini A., Hwang P., Hoffman H.J. et al.:Surgical treatment of epilepsy in tuberous sclerosis. Neurology, 1998, 51: 1263–1269.
Search in Google Scholar Back to article
Gurecki P.J., Holden K.R., Sahn E.E., Dyer D.S., Cure J.K.:Developmental neural abnormalities and seizures in epidermal nevus syndrome. Dev. Med. Child. Neurol., 1996, 38: 716–723.10.1111/j.1469-8749.1996.tb12141.x
Search in Google Scholar Back to article
Happle R.:Epidermal nevus syndrome. Semin. Dermatol., 1995, 14: 111–121.10.1016/S1085-5629(05)80006-9
Search in Google Scholar Back to article
Hennel S.J., Ekkert P.G., Volpe J.J., Inder T.E.:Insights into the pathogenesis of cerebral lesions in incontinentia pigmenti. Pediatr. Neurol., 2003, 29: 148–150.10.1016/S0887-8994(03)00150-4
Search in Google Scholar Back to article
Hsieh H.Y., Fung H.C., Wang C.J., Chin S.C., Wu T.:Epileptic seizures in neurofibromatosis type 1 are related to intracranial tumors but not to neurofibromatosis bright objects. Seizure, 2011, 20: 606–611.10.1016/j.seizure.2011.04.01621621428
Search in Google Scholar Back to article
Humphrey A., MacLean C., Ploubidis GB., Granader Y., Clifford M., Haslop M. et al.:Intellectual development before and after the onset of infantile spasms: a controlled prospective longitudinal study in tuberous sclerosis. Epilepsia, 2014, 55: 108–116. Hyman S.L., Gill D.S., Shores E.A., Steinberg A., Joy P., Gibikote S.V. et al.:Natural history of cognitive deficits and their relationship to MRI T2-hyperintensities in NF1. Neurology, 2003, 60: 1139–1145.
Search in Google Scholar Back to article
Ito M.:Studies of melanin IX. Incontinentia pigmenti achromians, a singular case of naevus depigmentosis systematicus bilateralis. Tohoku J. Exp. Med., 1952, 55: 57–59.
Search in Google Scholar Back to article
Jagtap S., Srinivas G., Harsha K.J., Radhakrishnan N., Radhakrishnan A. et al.:Sturge-Weber syndrome: clinical spectrum, disease course, and outcome of 30 patients. J. Child. Neurol., 2013, 28: 725–731.10.1177/0883073812451326
Search in Google Scholar Back to article
Jansen F.E., van Huffelen A.C., Algra A., van Nieuwenhuizen O.:Epilepsy surgery in tuberous sclerosis: a systematic review. Epilepsia, 2007, 48: 1477–1484.10.1111/j.1528-1167.2007.01117.x
Search in Google Scholar Back to article
Jóźwiak J., Jóźwiak S., Włodarski P.:Possible mechanisms of disease development in tuberous sclerosis. Lancet Oncology, 2008, 9: 73–79.10.1016/S1470-2045(07)70411-4
Search in Google Scholar Back to article
Jóźwiak S., Kossoff E.H., Kotulska-Jóźwiak K.:Dietary treatment of epilepsy: rebirth of an ancient treatment. Neurol. Neurochir. Pol., 2011a, 45: 370–378.10.1016/S0028-3843(14)60108-0
Search in Google Scholar Back to article
Jóźwiak S., Kotulska K., Domańska-Pakieła D., Łojszczyk B., Syczewska M., Chmielewski D. et al.:Antiepileptic treatment before the onset of seizures reduces epilepsy severity and risk of mental retardation in infants with tuberous sclerosis complex. Eur. J. Paediatr. Neurol., 2011b, 15: 424–431.10.1016/j.ejpn.2011.03.01021507691
Search in Google Scholar Back to article
Jóźwiak S.:Epilepsy and mental retardation in tuberous sclerosis complex – can we prevent them? In: T. Takahashi and Y. Fukuyama, Biology of Seizure Susceptibility in Developing Brain, John Libbey Eurotext, Montrouge 2008.
Search in Google Scholar Back to article
Kossoff E.H., Thiele E.A., Pfeifer H.H., McGrogan J.R., Freeman J.M.:Tuberous sclerosis complex and the ketogenic diet. Epilepsia, 2005, 46: 1684–1686.10.1111/j.1528-1167.2005.00266.x16190943
Search in Google Scholar Back to article
Kossoff E.H., Buck C., Freeman J.M.:Outcomes of 32 hemi-spherectomies for Sturge-Weber syndrome worldwide. Neurology, 2002, 59: 1735–1738.10.1212/01.WNL.0000035639.54567.5C
Search in Google Scholar Back to article
Kossoff E.H., Ferenc L., Comi A.M.:An infantile-onset, severe, yet sporadic seizure pattern is common in Sturge-Weber syndrome. Epilepsia, 2009, 50: 2154–2157.10.1111/j.1528-1167.2009.02072.x19389148
Search in Google Scholar Back to article
Kothare S.V., Singh K., Chalifoux J.R., Staley B.A., Weiner H.L., Menzer K. et al.:Severity of manifestations in tuberous sclerosis complex in relation to genotype. Epilepsia, 2014, Jun 10. doi: 10.1111/epi.12680. [Epub ahead of print].10.1111/epi.1268024917535
Search in Google Scholar Back to article
Kotulska K., Chmielewski D., Borkowska J., Jurkiewicz E., Kuczyński D., Kmieć T. et al.:Long-term effect of everolimus on epilepsy and growth in children under 3 years of age treated for subependymal giant cell astrocytoma associated with tuberous sclerosis complex. Eur. J. Paediatr. Neurology., 2013, 17: 479–485.10.1016/j.ejpn.2013.03.00223567018
Search in Google Scholar Back to article
Krsek P., Jahodova A., Kyncl M., Kudr M., Komarek V., Jezdik P. et al.:Predictors of seizure-free outcome after epilepsy surgery for pediatric tuberous sclerosis complex. Epilepsia, 2013, 54: 1913–1921.10.1111/epi.12371
Search in Google Scholar Back to article
Krueger D.A., Care M.M., Holland K., Agricola K., Tudor C., Mangeshkar P. et al.:Everolimus for subependymal giantcell astrocytomas in tuberous sclerosis. N. Engl. J. Med., 2010, 363: 1801–1811.10.1056/NEJMoa1001671
Search in Google Scholar Back to article
Krueger D.A., Wilfong AA., Holland-Bouley K., Anderson A.E., Agricola K., Tudor C. et al.:Everolimus treatment of refractory epilepsy in tuberous sclerosis complex. Ann. Neurol., 2013, 74: 679–687.10.1002/ana.23960
Search in Google Scholar Back to article
Kulkantrakorn K., Geller T.:Seizures in neurofibromatosis 1. Pediatr. Neurol., 1998, 19: 347–350.10.1016/S0887-8994(98)00075-7
Search in Google Scholar Back to article
Kwiatkowski D.J., Manning B.D.:Tuberous sclerosis: a GAP at the crossroads of multiple signaling pathways. Hum. Mol. Genet., 2005, 4: 251–258.10.1093/hmg/ddi26016244323
Search in Google Scholar Back to article
Lazarowski A., Ramos A.J., Garcia-Rivello H., Brusco A., Girardi E.:Neuronal and glial expression of the multidrug resistance gene product in an experimental epilepsy model. Cell. Mol. Neurobiol., 2004, 24: 77–85.10.1023/B:CEMN.0000012726.43842.d2
Search in Google Scholar Back to article
Ma T.S., Elliott R.E., Ruppe V., Devinsky O., Kuzniecky R., Weiner H.L., Carlson C.:Electrocorticographic evidence of perituberal cortex epileptogenicity in tuberous sclerosis complex. J. Neurosurg. Pediatr., 2012, 10: 376–382.10.3171/2012.8.PEDS128522998031
Search in Google Scholar Back to article
Maher C.O., Cohen-Gadol A.A., Raffel C.:Cortical resection for epilepsy in children with linear sebaceous nevus syndrome. Pediatr. Neurosurg., 2003, 39: 129–135.10.1159/00007164912876391
Search in Google Scholar Back to article
Major P., Thiele E.A.:Vagus nerve stimulation for intractable epilepsy in tuberous sclerosis complex. Epilepsy Behav., 2008, 13: 357–360.10.1016/j.yebeh.2008.04.00118468492
Search in Google Scholar Back to article
Menon G., Nair S., Sudhir J., Rao B.R., Mathew A., Bahuleyan B.:Childhood and adolescent meningiomas: a report of 38 cases and review of literature. Acta Neurochir., 2009, 151: 239–244. Menor F., Marti-Bonmati L., Arana E.:Neurofibromatosis type 1 in children: MR imaging and follow-up studies of central nervous system findings. Eur. J. Radiol., 1998, 26: 121–131. Meuwissen M., Mancini G.:Neurological findings in incontinentia pigmenti; a review. Eur. J. Med. Genet., 2012, 55: 323–331.
Search in Google Scholar Back to article
Muncy J., Butler I.J., Koenig M.K.:Rapamycin reduces seizures frequency in tuberous sclerosis complex. J. Child. Neurology, 2009, 24: 477.10.1177/0883073808324535307269619151365
Search in Google Scholar Back to article
Nehal K.S., PeBenito R., Orlow S.J.:Analysis of 54 cases of hypopigmentation and hyperpigmentation along the lines of Blaschko. Arch. Dermatol., 1996, 132: 1167–1170.10.1001/archderm.132.10.1167
Search in Google Scholar Back to article
North K.N.:Clinical aspects of neurofibromatosis 1. Eur. J. Paediatr. Neurol., 1998, 2: 223–231.10.1016/S1090-3798(98)80035-4
Search in Google Scholar Back to article
Northrup H., Krueger D.A.:International Tuberous Sclerosis Complex Consensus Group. Tuberous Sclerosis Complex Diagnostic Criteria Update: Recommendations of the 2012 International Tuberous Sclerosis Complex Consensus Conference. Pediatric Neurology, 2013, 49: 243–254.
Search in Google Scholar Back to article
O’Callaghan F.J., Harris T., Joinson C., Bolton P., Noakes M., Presdee D. et al.:The relation of infantile spasms, tubers, and intelligence in tuberous sclerosis complex. Arch. Dis. Child., 2004, 89: 530–533.10.1136/adc.2003.026815
Search in Google Scholar Back to article
Ostendorf A.P., Gutmann D.H., Weisenberg J.L.:Epilepsy in individuals with neurofibromatosis type 1. Epilepsia, 2013, 54: 1810–1814.10.1111/epi.12348
Search in Google Scholar Back to article
Parisi P., Bombardieri R., Curatolo P.:Current role of vigabatrin in infantile spasms. Eur. J. Paediatr. Neurol., 2007, 11: 331–336.10.1016/j.ejpn.2007.03.010
Search in Google Scholar Back to article
Pascual-Castroviejo I., Pascual-Pascual S.I., Velazquez-Fragua R., Viano J.:Sturge-Weber syndrome: study of 55 patients. Can. J. Neurol. Sci., 2008, 35: 301–307.10.1017/S0317167100008878
Search in Google Scholar Back to article
Pavonne L., Curatolo P., Rizzo R., Micali G., Incorpora G., Garg B.P. et al.:Epidermal nevus syndrome: a neurologic variant with hemimegalancephaly, gyral malformation, mental retardation, seizures and facial hemihypertrophy. Neurology, 1991, 41: 266–271.10.1212/WNL.41.2_Part_1.266
Search in Google Scholar Back to article
Perek-Polnik M., Jóźwiak S., Jurkiewicz E., Perek D., Kotulska K.:Effective everolimus treatment of inoperable, life-threatening subependymal giant cell astrocytoma and intractable epilepsy in a patient with tuberous sclerosis complex. Eur. J. Paediatr. Neurol., 2012, 16: 83–85.10.1016/j.ejpn.2011.09.006
Search in Google Scholar Back to article
Roach E.S.:Neurocutaneous syndromes. Pediatr. Clin. North. Am., 1992, 39: 591–620.10.1016/S0031-3955(16)38367-5
Search in Google Scholar Back to article
Rubi S., Costes N., Heckemann R.A., Bouvard S., Hammers A., Marti-Fuster B. et al.:Positron emission tomography with α-[11C]methyl-L-tryptophan in tuberous sclerosis complex-related epilepsy. Epilepsia, 2013, 54: 2143–2150.10.1111/epi.1241224304437
Search in Google Scholar Back to article
Shen M.H., Harper P.S., Upadhyaya M.:Molecular genetics of neurofibromatosis type 1 (NF1). J. Med. Genet., 1996, 33: 2–17. Shepherd C.W. Gomez M.R., Lie J.T, Crowson C.S.:Causes of death in patients with tuberous sclerosis. Mayo Clin. Proc., 1991, 66: 792–796.
Search in Google Scholar Back to article
Shirley M.D., Tang H., Gallione C.J., Baugher J.D., Frelin L. P., Cohen B. et al.:Sturge-Weber syndrome and port-wine stains caused by somatic mutation in GNAQ. N. Eng. J. Med., 2013, 368: 1971–1979.10.1056/NEJMoa1213507374906823656586
Search in Google Scholar Back to article
Sparagana S.P., Delgado M.R., Batchelor R.R., Roach E.S.:Seizure remission and antiepileptic drug discontinuation in children with tuberous sclerosis complex. Arch. Neurol., 2003, 60: 1286–1289.10.1001/archneur.60.9.128612975296
Search in Google Scholar Back to article
Sujansky E., Conradi S.:Outcome of Sturge-Weber syndrome in 52 adults. Am. J. Med. Genet., 1995, 57: 35–45.10.1002/ajmg.13205701107645596
Search in Google Scholar Back to article
Talos D.M., Sun H., Zhou X., Fitzgerald E.C., Jackson M.C., Klein P.M. et al.:The interaction between early life epilepsy and autistic-like behavioralconsequences: a rolefor the mammalian target of rapamycin (mTOR) pathway. PLoS One, 2012, 7: e35885.10.1371/journal.pone.0035885334233422567115
Search in Google Scholar Back to article
Thiele E.A.:Managing epilepsy in tuberous sclerosis complex. J. Child. Neurol., 2004, 19: 680–686.10.1177/0883073804019009080115563014
Search in Google Scholar Back to article
Ville D., Enjolras O., Chiron C., Dulac O.:Prophylactic antiepileptic treatment in Sturge-Weber disease. Seizure, 2002, 11: 145–150.10.1053/seiz.2001.062912018956
Search in Google Scholar Back to article
Vivarelli R., Grosso S., Calabrese F., Farnetani M., Galluzzi P., Vatti G.P. et al.:Epilepsy in neurofibromatosis 1. J. Child. Neurol., 2003, 18: 338–342.10.1177/0883073803018005050112822818
Search in Google Scholar Back to article
Webb D.W., Fryer A.E., Osborne J.P.:Morbidity associated with tuberous sclerosis: a population study. Dev. Med. Child. Neurol., 1996, 38: 146–155.10.1111/j.1469-8749.1996.tb12086.x8603782
Search in Google Scholar Back to article
Wheless J.W., Clarke D.F., Arzimanoglou A., Carpenter D.:Treatment of pediatric epilepsy: European expert opinion, 2007. Epileptic Disord., 2007, 9: 353–412.
Search in Google Scholar Back to article
Wiederholt W.C., Gomez M.R., Kurland L.T.:Incidence and prevalence of tuberous sclerosis in Rochester, Minnesota, 1950 through 1982. Neurology, 1985, 35: 600–603.10.1212/WNL.35.4.600
Search in Google Scholar Back to article
Wong M.:Mammalian target of rapamycin (mTOR) inhibition as a potential antiepileptogenic therapy: from tuberous sclerosis to common acquired epilepsies. Epilepsia, 2010, 51: 27–36.10.1111/j.1528-1167.2009.02341.x302251319817806
Search in Google Scholar Back to article
Wu J.Y., Salamon N., Kirsch H.E., Mantle M.M., Nagarajan S.S., Kurelowech L. et al.:Noninvasive testing, early surgery and seizure freedom in tuberous sclerosis complex. Neurology, 2010, 74: 392–398.10.1212/WNL.0b013e3181ce5d9e281600720124204
Search in Google Scholar Back to article
Yates J.R.:Tuberous sclerosis. Eur. J. Hum. Genet., 2006, 14: 1065–1073.10.1038/sj.ejhg.520162516868562
Search in Google Scholar Back to article
Zhang B., McDaniel S.S., Rensing N.R., Wong M.:Vigabatrin inhibits seizures and mTOR pathway activation in a mouse model of tuberous sclerosis complex. PLoS One, 2013, 8: e57445.10.1371/journal.pone.0057445357771023437388
Search in Google Scholar Back to article

Recent advances in pathophysiology studies and treatment of epilepsy in neurocutaneous disorders

Abstract

Introduction

Aim

Material and methods

Discussion and conclusions

Paradigm

My account