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

• Autorzy: Krzysztof Sadowski , Sergiusz Jóźwiak
• Języki publikacji: EN

Abstrakty

EN

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.

Słowa kluczowe

EN

epilepsy; neurocutaneous disorders; tuberous sclerosis; pathogenesis; treatment recommendation

• Czasopismo: Journal of Epileptology
• Rocznik: 2014
• Tom: 22
• Numer: 2
• Strony: 99-108

Daty

wydano

2014-12-01

otrzymano

2014-07-24

zaakceptowano

2014-10-03

online

2015-03-01

Twórcy

autor

Krzysztof Sadowski

• Department of Neurology, Health Science Faculty, Medical University of Warsaw,

autor

Sergiusz Jóźwiak

• Department of Neurology and Epileptology, The Children's Memorial Health Institute, Warsaw

Bibliografia

• 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.[Crossref][PubMed]
• Arun D., Gutmann D.H.:Recent advances in neurofibromatosis 1. Curr. Opin. Neurol., 2004, 17: 101–105.[Crossref]
• 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.[Crossref]
• 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.[Crossref]
• Bebin E.M., Gomez M.R.:Prognosis in Sturge-Weber disease: comparison of unihemisspheric and bihemispheric involvement. J. Child. Neurol., 1992, 3: 181–184.[Crossref]
• 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.[Crossref]
• 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.
• Comi A.M.:Update on Sturge-Weber syndrome: diagnosis, treatment, quantitative measures, and controversies. Lymphat. Res. Biol., 2007, 5: 257–264.[PubMed][Crossref]
• 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.[PubMed][Crossref]
• Crumrine P.K.:Mamagement of seizures in Lennox-Gastaut syndrome. Paediatr. Drugs., 2011, 13: 107–118.[Crossref]
• Curatolo P., Bombardieri R., Jóźwiak S.:Tuberous sclerosis. Lancet, 2008, 372: 657–668.[Crossref][PubMed]
• 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.
• 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.[PubMed]
• 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.[Crossref]
• 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.[Crossref][PubMed]
• 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.[Crossref]
• 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.
• 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.[Crossref]
• 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.[Crossref][PubMed]
• 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.[PubMed][Crossref]
• 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.[PubMed][Crossref]
• Happle R.:Epidermal nevus syndrome. Semin. Dermatol., 1995, 14: 111–121.[PubMed][Crossref]
• 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.[PubMed][Crossref]
• 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.[PubMed][Crossref]
• 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.[Crossref][PubMed]
• 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.
• 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.
• 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.[Crossref]
• 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.[PubMed][Crossref]
• Jóźwiak J., Jóźwiak S., Włodarski P.:Possible mechanisms of disease development in tuberous sclerosis. Lancet Oncology, 2008, 9: 73–79.[Crossref]
• Jóźwiak S., Kossoff E.H., Kotulska-Jóźwiak K.:Dietary treatment of epilepsy: rebirth of an ancient treatment. Neurol. Neurochir. Pol., 2011a, 45: 370–378.[PubMed]
• 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.
• 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.
• 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.[Crossref][PubMed]
• Kossoff E.H., Buck C., Freeman J.M.:Outcomes of 32 hemi-spherectomies for Sturge-Weber syndrome worldwide. Neurology, 2002, 59: 1735–1738.[Crossref]
• 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.[Crossref][PubMed]
• 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].[Crossref]
• 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.[Crossref]
• 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.[Crossref][PubMed]
• Krueger D.A., Care M.M., Holland K., Agricola K., Tudor C., Mangeshkar P. et al.:Everolimus for subependymal giant-cell astrocytomas in tuberous sclerosis. N. Engl. J. Med., 2010, 363: 1801–1811.[Crossref]
• 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.[PubMed][Crossref]
• Kulkantrakorn K., Geller T.:Seizures in neurofibromatosis 1. Pediatr. Neurol., 1998, 19: 347–350.[Crossref]
• Kwiatkowski D.J., Manning B.D.:Tuberous sclerosis: a GAP at the crossroads of multiple signaling pathways. Hum. Mol. Genet., 2005, 4: 251–258.[Crossref]
• 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.[Crossref]
• 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.[Crossref]
• 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.[Crossref][PubMed]
• Major P., Thiele E.A.:Vagus nerve stimulation for intractable epilepsy in tuberous sclerosis complex. Epilepsy Behav., 2008, 13: 357–360.[Crossref][PubMed]
• 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.[Crossref]
• 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.[Crossref][PubMed]
• Meuwissen M., Mancini G.:Neurological findings in incontinentia pigmenti; a review. Eur. J. Med. Genet., 2012, 55: 323–331.[Crossref]
• Muncy J., Butler I.J., Koenig M.K.:Rapamycin reduces seizures frequency in tuberous sclerosis complex. J. Child. Neurology, 2009, 24: 477.[Crossref]
• 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.[Crossref]
• North K.N.:Clinical aspects of neurofibromatosis 1. Eur. J. Paediatr. Neurol., 1998, 2: 223–231.
• 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.[Crossref]
• 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.[Crossref]
• Ostendorf A.P., Gutmann D.H., Weisenberg J.L.:Epilepsy in individuals with neurofibromatosis type 1. Epilepsia, 2013, 54: 1810–1814.[Crossref]
• Parisi P., Bombardieri R., Curatolo P.:Current role of vigabatrin in infantile spasms. Eur. J. Paediatr. Neurol., 2007, 11: 331–336.
• 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.[Crossref]
• 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.[Crossref]
• 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.
• Roach E.S.:Neurocutaneous syndromes. Pediatr. Clin. North. Am., 1992, 39: 591–620.[PubMed]
• 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.[Crossref]
• Shen M.H., Harper P.S., Upadhyaya M.:Molecular genetics of neurofibromatosis type 1 (NF1). J. Med. Genet., 1996, 33: 2–17.[Crossref]
• 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.[PubMed][Crossref]
• 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.[Crossref]
• 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.
• Sujansky E., Conradi S.:Outcome of Sturge-Weber syndrome in 52 adults. Am. J. Med. Genet., 1995, 57: 35–45.[Crossref]
• 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.
• Thiele E.A.:Managing epilepsy in tuberous sclerosis complex. J. Child. Neurol., 2004, 19: 680–686.
• Ville D., Enjolras O., Chiron C., Dulac O.:Prophylactic antiepileptic treatment in Sturge-Weber disease. Seizure, 2002, 11: 145–150.[PubMed][Crossref]
• 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.[Crossref]
• 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.[Crossref][PubMed]
• Wheless J.W., Clarke D.F., Arzimanoglou A., Carpenter D.:Treatment of pediatric epilepsy: European expert opinion, 2007. Epileptic Disord., 2007, 9: 353–412.[PubMed]
• 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.[Crossref]
• 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.[Crossref][PubMed]
• 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.[Crossref][PubMed]
• Yates J.R.:Tuberous sclerosis. Eur. J. Hum. Genet., 2006, 14: 1065–1073.[Crossref]
• 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.

Identyfikatory

DOI

10.1515/joepi-2015-0017