Management of CNS-related disease manifestations in patients with tuberous sclerosis complex

Current Treatment Options in Neurology

Volumn 15, Issue 5, 2013, Pages 618-633

  Krueger, Darcy A ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

CNS; Epilepsy; Everolimus; Infantile spasms; Management; mTOR; Sirolimus; Subependymal giant cell astrocytoma (SEGA); Treatment; TSC associated neuropsychiatric disorder (TAND); Tuberous sclerosis; Vigabatrin

Indexed keywords

AMPRENAVIR; ANTICONVULSIVE AGENT; APREPITANT; ATAZANAVIR; ATYPICAL ANTIPSYCHOTIC AGENT; CLARITHROMYCIN; CORTICOTROPIN; CYTOCHROME P450 3A4; ERYTHROMYCIN; ETIRACETAM; EVEROLIMUS; FLUCONAZOLE; FOSAMPRENAVIR; INDINAVIR; ITRACONAZOLE; KETOCONAZOLE; LAMOTRIGINE; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; NEFAZODONE; NELFINAVIR; OXCARBAZEPINE; RAPAMYCIN; RITONAVIR; SAQUINAVIR; SEROTONIN UPTAKE INHIBITOR; TOPIRAMATE; UNINDEXED DRUG; VERAPAMIL; VIGABATRIN; VORICONAZOLE;

ADOLESCENCE; ADULTHOOD; AGE; ARTICLE; BRAIN SURGERY; CHILDHOOD; CHOLESTEROL BLOOD LEVEL; CLINICAL FEATURE; DIAGNOSTIC IMAGING; DIAGNOSTIC TEST; DIET THERAPY; DISEASE ASSOCIATION; DISEASE SEVERITY; DRUG BLOOD LEVEL; DRUG COST; DRUG DOSE INCREASE; DRUG MEGADOSE; ELECTROENCEPHALOGRAM; EPILEPSY; EPILEPSY SURGERY; HUMAN; INFANTILE SPASM; INFECTION; LIFESTYLE MODIFICATION; MENTAL DISEASE; MOUTH DISEASE; MOUTH ULCER; MUSCLE SPASM; NEUROLOGICAL COMPLICATION; NUCLEAR MAGNETIC RESONANCE IMAGING; OPPORTUNISTIC INFECTION; PATIENT CARE; PRENATAL DIAGNOSIS; SEIZURE; SIDE EFFECT; SOMNOLENCE; SUBEPENDYMAL GIANT CELL ASTROCYTOMA; TREATMENT CONTRAINDICATION; TREATMENT INDICATION; TUBEROUS SCLEROSIS; VAGUS NERVE STIMULATION; VISUAL IMPAIRMENT; WOUND HEALING IMPAIRMENT;

EID: 84885189214     PISSN: 10928480     EISSN: 15343138     Source Type: Journal    
DOI: 10.1007/s11940-013-0249-2     Document Type: Article

References (82)

1. Bourneville D-M. Encéphalite ou sclérose tubéreuse des circonvolutions cérébrales. Encéphalite ou sclérose tubéreuse des circonvolutions cérébrales [Encephalitis or tuberous sclerosis of the cerebral convolutions]. Archives de Neurologie, Paris. 1881;1:390-412.
2. Von Recklinghausen F. Ein Herz von einem Nuegeborene welches mehrere theils nachaussen, theils nachden Höhlein prominirende Tumoren (Myomen) trug. Ein Herz von einem Nuegeborene welches mehrere theils nachaussen, theils nachden Höhlein prominirende Tumoren (Myomen) trug [A heart of a newborn with partial external and internal prominent tumors (fibroids)]. Monatschr Gebursheklkd. 1862;20:1-2.
3. O'Callaghan F, Shiell A, Osborne J, Martyn C. Prevalence of tuberous sclerosis estimated by capture-recapture analysis. Lancet. 1998;352:318-9.
4. European Chromosome 16 Tuberous Sclerosis Consortium. Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell. 1993;75:1305-15.
5. van Slegtenhorst M, deHoogt R, Hermans C, Henske E, Short M, et al. Identification of the tuberous sclerosis gene TSC1 on chromosome 9q34. Science. 1997;277:805-8.
6. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J. Rheb binds and regulates the mTOR kinase. Curr Biol. 2005;15:702-13.
7. Franz D, Belousova E, Sparagana S, Bebin E, Frost M, et al. Efficacy and safety of everolimus for subependymal giant cell astrocytomas associate702-71d with tuberous sclerosis complex (EXIST-1): a multicentre, randomised, placebo-controlled phase 3 trial. Lancet. 2012;381:125-32. This article provides definitive evidence of the benefit of everolimus for the treatment of SEGA in a randomized, double-blinded placebo-controlled design. All of the patients in the treatment group demonstrated some degree of benefit, whereas tumor progression was only observed in the placebo group. Class I evidence.
8. Franz DN, Leonard J, Tudor C, Chuck G, Care M, et al. Rapamycin Causes Regression of Astrocytomas in Tuberous Sclerosis Complex. Ann Neurol. 2006;59:490-8.
9. Krueger D, Care M, Agricola K, Tudor C, Mays M, et al. Everolimus long-term safety and efficacy in subependymal giant-cell astrocytoma. Neurology. 2012;80:574-80. This article provides most up to date evidence of long-term safety and efficacy of everolimus for medical management of SEGA. Treatment continues to be well-tolerated and prevents tumor progression median treatment duration of 34.2 months. Class III evidence.
10. Krueger DA, Care MM, Holland K, Agricola K, Tudor C, et al. Everolimus for subependymal giant-cell astrocytomas in tuberous sclerosis. N Engl J Med. 2010;363:1801-11.
11. Bissler JJ, Kingswood JC, Radzikowska E, Zonnenberg BA, Frost M, et al. Everolimus for angiomyolipoma associated with tuberous sclerosis complex or sporadic lymphangioleiomyomatosis: a multicentre, randomised, double-blind, placebo-controlled trial. Lancet. 2013;[Epub ahead of print].
12. Bissler JJ, McCormack FX, Young LR, Elwing JM, Chuck G, et al. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N Engl J Med. 2008;358:140-51.
13. Dabora SL, Franz DN, Ashwal S, Sagalowsky A, DiMario Jr FJ, et al. Multicenter phase 2 trial of sirolimus for tuberous sclerosis: Kidney angiomyolipomas and other tumors regress and VEGF- D levels decrease. PLoS ONE. 2011;6.
14. Davies DM, De Vries PJ, Johnson SR, McCartney DL, Cox JA, et al. Sirolimus therapy for angiomyolipoma in tuberous sclerosis and sporadic lymphangioleiomyomatosis: a phase 2 trial. Clin Cancer Res. 2011;17:4071-81.
15. McCormack F, Inoue Y, Moss J, Singer L, Strange C, et al. Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N Engl J Med. 2011;364:1595-606.
16. Foster R, Bint L, Halbert A. Topical 0.1% rapamycin for angiofibromas in paediatric patients with tuberous sclerosis: a pilot study of four patients. Australas J Dermatol. 2012;53:52-6.
17. Haemel A, O'Brian A, Teng J. Topical rapamycin: a novel approach to facial angiofibromas in tuberous sclerosis. Arch Dermatol. 2010;146:715-8.
18. Koenig M, Hebert A, Roberson J, Samueals J, Slopis J, et al. Topical rapamycin therapy to alleviate the cutaneous manifestations of tuberous sclerosis complex: a double-blind, randomized, controlled trial to evaluate the safety and efficacy of topical applied rapamycin. Drugs R&D. 2012;12:121-6.
19. Mutizwa M, Berk D, Anadkat M. Treatment of facial angiofibromas with topical application of oral rapamycin solution (1mgmL(-1)) in two patients with tuberous sclerosis. Br J Dermatol. 2011;165:922-3.
20. Demir H, Ekici F, Yazal Erdem A, Emir S, Tunç B. Everolimus: a challenging drug in the treatment of multifocal inoperable cardiac rhabdomyoma. Pediatrics. 2012;130:e243-7.
21. Tiberio D, Franz D, Phillips J. Regression of a cardiac rhabdomyoma in a patient receiving everolimus. Pediatrics. 2011;127:e1335-7.
22. Krueger D, Wilfong A, Holland-Bouley K, Anderson A, Agricola K, et al. Everolimus treatment of refractory epilepsy in tuberous sclerosis complex. Ann Neurol. 2013. doi: 10.1002/ana.23960.
23. Adams R, Victor M. Principles of neurology. New York: McGraw-Hill; 1985. p. 1186.
24. Menkes J, Maria B. Neurocutaneous syndromes. In: Menkes J, Sarnat H, editors. Child Neurology. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2000. p. 865-72.
25. Zhou J, Shrikhande G, Xu J, McKay R, Burns D, et al. Tsc1 mutant neural stem/progenitor cells exhibit migration deficits and give rise to subependymal lesions in the lateral ventricle. Genes Dev. 2011;25:1595-600.
26. Way S, McKenna III J, Mietzsch U, Reith R, Wu H, et al. Loss of Tsc2 in radial glia models the brain pathology of tuberous sclerosis complex in the mouse. Hum Mol Gen. 2009;18:1252-65.
27. Carlson B, Houser O, Gomez M. Brain imaging in the tuberous sclerosis complex. In: Gomez M, Sampson J, Whittemore V, editors. Tuberous sclerosis complex. 3rd ed. New York: Oxford University Press; 1999. p. 85-100.
28. Roach ES, Gomez MR, Northrup H. Tuberous sclerosis complex consensus conference: revised clinical diagnostic criteria. J Child Neurol. 1998;13:624-8.
29. Inoue Y, Nemoto Y, Murata R, Tashiro T, Shakudo M, et al. CT and MR imaging of cerebral tuberous sclerosis. Brain Dev. 1998;20:209-21.
30. Kalantari BN, Salamon N. Neuroimaging of tuberous sclerosis: spectrum of pathologic findings and frontiers in imaging. Am J Roentgenol. 2008;190:W304-9.
31. Crino P, Mehta R, Vinters H. Pathogenesis of TSC in the brain. In: Kwiatkowsi D, Whittemore V, Thiele E, editors. Tuberous sclerosis complex: genes, clinical features, and therapeutics. Weinheim: Wiley-Blackwell; 2010. p. 285-309.
32. Kim SK, Wang KC, Cho BK, Jung HW, Lee YJ, et al. Biological behavior and tumorigenesis of subependymal giant cell astrocytomas. J Neuro-Oncol. 2001;52:217-25.
33. Adriaensen ME, Schaefer-Prokop CM, Stijnen T, Duyndam DA, Zonnenberg BA, et al. Prevalence of subependymal giant cell tumors in patients with tuberous sclerosis and a review of the literature. Eur J Neurol. 2009;16:691-6.
34. Phi JH, Park SH, Chae JH, Hong KH, Park SS, et al. Congenital subependymal giant cell astrocytoma: clinical considerations and expression of radial glial cell markers in giant cells. Child Nerv Syst. 2008;24:1499-503.
35. Raju GP, Urion DK, Sahin M. Neonatal Subependymal Giant Cell Astrocytoma: new case and review of literature. Pediatr Neurol. 2007;36:128-31.
36. Shepherd CW, Scheithauer B, Gomez MR. Brain tumors in tuberous sclerosis. A clinicopathologic study of the Mayo Clinic experience. Ann N Y Acad Sci. 1991;615:378-9.
37. Buccoliero A, Franchi A, Castiglione F, Gheri C, Mussa F, et al. Subependymal giant cell astrocytoma (SEGA): is it an astrocytoma? Morphological, immunohistochemical and ultrastructural study. Neuropathology. 2009;29:25-30.
38. Cuccia V, Zuccaro G, Sosa F, Monges J, Lubienieky F, et al. Subependymal giant cell astrocytoma in children with tuberous sclerosis. Child Nerv Syst. 2003;19:232-43.
39. The International Tuberous Sclerosis Complex Consensus Group. "Recommendations for surveillance and management in tuberous sclerosis complex: 2012 update of the International Tuberous Sclerosis Complex Consensus Conference." Presented at the 2013 International Research Conference on Tuberous Sclerosis Complex and Related Disorders, Washington, DC, June 20-23, 2014.
40. Thiele EA. Managing epilepsy in tuberous sclerosis complex. J Child Neurol. 2004;19:680-6.
41. JóÅwiak S, Kotulska K, Domańska-Pakieła D, Łojszczyk B, Syczewska M, 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 Paediat Neurol. 2011;15:424-31. This paradigm shifting article introduces a prospective, preventative approach towards seizure control rather than the traditional reactionary approach of waiting until after the onset of clinical seizures in infants with TSC. As a result, those infants treated prospectively demonstrated improved long-term seizure control and developmental progress. Class III evidence.
42. Curatolo P, Verdecchia M, Bombardieri R. Tuberous sclerosis complex: a review of neurological aspects. Eur J Paediat Neurol. 2002;6:15-23.
43. de Vries P. Neurodevelopmental, Psychiatric and Cognitive Aspects of Tuberous Sclerosis Complex. In: Kwiatkowsi DJ, Whittemore VH, Thiele EA, editors. Tuberous Sclerosis Complex. Weinheim: Wiley-Blackwell; 2010. p. 229-68.
44. Leclezio L, de Vries P. The Tuberous Sclerosis Complex Associated Neuropsychiatrif Disorders (TAND) Checklist- Pilot validation of a new screening tool for neurophsyciatric manifestations of TSC. Washington, DC.2013.
45. De Vries P, Humphrey A, McCartney D, Prather P, Bolton P, et al. Consensus clinical guidelines for the assessment of cognitive and behavioral problems in Tuberous Sclerosis. Eur Child Adolesc Psychiatr. 2005;14:183-90.
46. Stafstrom CE, Bough KJ. The Ketogenic Diet for the Treatment of Epilepsy: a challenge for nutritional neuroscientists. Nutr Neurosci. 2003;6:67-79.
47. Kossoff E, Thiele E, Pfeifer H, McGrogan J, Freeman J. Tuberous sclerosis complex and the ketogenic diet. Epilepsia. 2005;46:1684-6.
48. Coppola G, Klepper J, Ammendola E, Fiorillo M, Corte R, et al. The effects of the ketogenic diet in refractory partial seizures with reference to tuberous sclerosis. Eur J Paediat Neurol. 2006;10:148-51.
49. Larson AM, Pfeifer HH, Thiele EA. Low glycemic index treatment for epilepsy in tuberous sclerosis complex. Epilepsy Res. 2012;99(1-2):180-2
50. Agricola K, Tudor C, Krueger D, Franz D. Nursing implications for the lifelong management of tuberous sclerosis complex. J Neurosci Nurs. 2013(in press).
51. Meikle L, Pollizzi K, Egnor A, Kramvis I, Lane H, et al. Response of a neuronal model of tuberous sclerosis to mammalian target of rapamycin (mTOR) inhibitors: effects on mTORC1 and Akt signaling lead to improved survival and function. J Neurosci. 2008;28:5422-32.
52. Meikle L, Talos D, Onda H, Pollizzi K, Rotenberg A, et al. A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival. J Neurosci. 2007;27:5546-58.
53. Muncy J, Butler IJ, Koenig M. Rapamycin reduces seizure frequency in tuberous sclerosis complex. J Child Neurol. 2009;24:477.
54. Zeng L, Rensing N, Wong M. The mammalian target of rapamycin signaling pathway mediates epileptogenesis in a model of temporal lobe epilepsy. J Neurosci. 2009;29:6964-72.
55. Zeng LH, Xu L, Gutmann DH, Wong M. Rapamycin prevents epilepsy in a mouse model of tuberous sclerosis complex. Ann Neurol. 2008;63:444-53.
56. McDaniel S, Rensing N, Thio L, Yamada K, Wong M. The ketogenic diet inhibits the mammalian target of rapamycin (mTOR) pathway. Epilepsia. 2011;52:e7-11.
57. Ehninger D, Han S, Shilyansky C, Zhou Y, Li W, et al. Reversal of learning deficits in a Tsc2+/- mouse model of tuberous sclerosis. Nat Med. 2008;14:843-8.
58. Ehninger D, Silva AJ. Rapamycin for treating Tuberous sclerosis and Autism spectrum disorders. Trends Mol Med. 2011;17:78-87.
59. Go C, Mackay M, Weiss S, Stephens D, Addams-Webber T, et al. Evidence-based guideline update: medical treatment of infantile spasms. Neurology. 2012;78:1974-80.
60. Camposano SE, Major P, Halpern E, Thiele EA. Vigabatrin in the treatment of childhood epilepsy: a retrospective chart review of efficacy and safety profile. Epilepsia. 2008;49:1186-91.
61. Greiner H, Lynch E, Fordyce S, Agricola K, Tudor C, et al. Vigabatrin for childhood partial-onset epilepsies. Pediat Neurol. 2012;46:83-8.
62. Kinirons P, Cavalleri G, O'Rourke D, Doherty C, Reid I, et al. Vigabatrin retinopathy in an Irish cohort: lack of correlation with dose. Epilepsia. 2006;47:311-7.
63. Jammoul F, Wang Q, Nabbout R, Coriat C, Duboc A, et al. Taurine deficiency is a cause of vigabatrin-induced retinal phototoxicity. Ann Neurol. 2009;65:98-107.
64. Collins J, Tudor C, Leonard J, Chuck G, Franz D. Levetiracetam as adjunctive antiepileptic therapy for patients with tuberous sclerosis complex: a retrospective open-label trial. J Child Neurol. 2006;21:53-7.
65. Franz D, Leonard J, Tudor C, Chuck G, Egelhoff J. Levetiracetam therapy of epilepsy in tuberous sclerosis. J Child Neurol. 2001;16:679.
66. Franz D, Leonard J, Tudor C, Chuck G, Egelhoff J. Oxcarbazepine therapy of epilepsy in tuberous sclerosis. J Child Neurol. 2001;16:680.
67. Franz D, Tudor C, Leonard J. Topiramate as therapy for tuberous sclerosis complex-associated seizures. Epilepsia. 2000;41:87.
68. Franz D, Tudor C, Leonard J, Egelhoff J, Byars A, et al. Lamotrigine therapy of epilepsy in tuberous sclerosis. Epilepsia. 2001;42:935-40.
69. Franz DN, Tudor C, Leonard J, Egelhoff JC, Byars A, et al. Lamotrigine therapy of epilepsy in tuberous sclerosis. Epilepsia. 2001;42:935-40.
70. Chung T, Lynch E, Fiser C, Nelson D, Agricola K, et al. Psychiatric comorbidity and treatment response in patients with tuberous sclerosis complex. Ann Clin Psychiatr. 2011;23:263-9.
71. Krueger DA, Franz DN. Current management of tuberous sclerosis complex. Pediatr Drugs. 2008;10:299-313.
72. Jozwiak J, Jozwiak S, Oldak M. Molecular activity of sirolimus and its possible application in tuberous sclerosis treatment. Med Res Rev. 2006;26:160-80.
73. Wheless J, Ramsay R, Collins S. Vigabatrin. Neurotherapeutics. 2007;4:163-72.
74. Berhouma M. Management of subependymal giant cell tumors in tuberous sclerosis complex: the neurosurgeon's perspective. World J Pediatr. 2010;6:103-10.
75. de Ribaupierre S, Dorfmüller G, Bulteau C, Fohlen M, Pinard J, et al. Subependymal giant-cell astrocytomas in pediatric tuberous sclerosis disease: when should we operate? Neurosurgery. 2007;60:83-9.
76. Moavero R, Pinci M, Bombardieri R, Curatolo P. The management of subependymal giant cell tumors in tuberous sclerosis: a clinician's perspective. Child Nervous Syst. 2011;27:1203-10.
77. Sun P, Kohrman M, Liu J, Guo A, Rogerio J, et al. Outcomes of resecting subependymal giant cell astrocytoma (SEGA) among patients with SEGA-related tuberous sclerosis complex: a national claims database analysis. Curr Med Res Opin. 2012;28:657-63.
78. Franz D, Agricola KD, Tudor C, Krueger D. Everolimus for tumor recurrence after surgical resection for subependymal giant cell astrocytoma assocaited with tuberous sclerosis complex. J Child Neurol. 2012;28:602-7.
79. Connolly MB, Hendson G, Steinbok P. Tuberous sclerosis complex: a review of the management of epilepsy with emphasis on surgical aspects. Child Nerv Syst. 2006;22:896-908.
80. Koh S, Jayakar P, Dunoyer C, Whiting SE, Resnick TJ, et al. Epilepsy surgery in children with tuberous sclerosis complex: presurgical evaluation and outcome. Epilepsia. 2000;41:1206-13.
81. Weiner HL, Ferraris N, LaJoie J, Miles D, Devinsky O. Epilepsy surgery for children with tuberous sclerosis complex. J Child Neurol. 2004;19:687-9.
82. Elliott RE, Carlson C, Kalhorn SP, Moshel YA, Weiner HL, et al. Refractory epilepsy in tuberous sclerosis: vagus nerve stimulation with or without subsequent resective surgery. Epilepsy Behav. 2009;16:454-60.