Tuberous sclerosis complex, Clinic and pathology manifestations, Mini -review
Abstract
Tuberous sclerosis complex (TSC) is an autosomal dominant neurocutaneous syndrome that affects almost all of the organs of the body, including the brain, heart, lungs, liver, and kidneys. Brain tumors in TSC patients include cortical tubers, subependymal nodules (SENs), and Subependymal giant cell astrocytomas (SEGAs). Seizures that occur in 92% of patients with TSC are an important cause of sudden deaths in them. Other organ involvement includes renal angiomyolipomas, lymphangioleiomyomatosis, cardiac rhabdomyomas, and cutaneous manifestations (hypomelanotic macules, angiofibromas, ungual fibromas, shagreen patch, and 'confetti' skin lesions). There is a criterion for tuberous sclerosis complex that consists of 11 major and 6 minor clinical features that diagnosis occurs based on it. The best way for definitive diagnosis of TSC in a patient is using genetic tests and histopathology. Immunohistochemistry is a helpful method in confirming the diagnosis of brain tumors in TSC. Immunostaining of SEGA shows positivity for GFAP and S-100 protein while neurofilament and synaptophysin are negative. Ki-67, which indicates nuclear proliferation, has a low proliferation index in immunostain. At the beginning of aggression the tumor or manifestation of hydrocephalus and symptoms of rising intracranial pressure and focal neurologic deficit, surgery is a necessity and can improve outcome. The aim of this study is a concise review of literature for clinicians and pathologists for better diagnosis and management of disease with variable manifestation of this disease with a focus on the histopathological findings of brain involvement.
1. Fohlen M, Ferrand-Sorbets S, Delalande O, Dorfmüller G. Surgery for subependymal giant cell astrocytomas in children with tuberous sclerosis complex. Childs Nerv Syst. 2018;34(8):1511-9.
2. Jiang T, Du J, Raynald, Wang J, Li C. Presurgical Administration of mTOR Inhibitors in Patients with Large Subependymal Giant Cell Astrocytoma Associated with Tuberous Sclerosis Complex. World Neurosurg. 2017;107:1053.e1-.e6.
3. Katz JS, Frankel H, Ma T, Zagzag D, Liechty B, Zeev BB, et al. Unique findings of subependymal giant cell astrocytoma within cortical tubers in patients with tuberous sclerosis complex: a histopathological evaluation. Childs Nerv Syst. 2017;33(4):601-7.
4. Mizuguchi M. Abnormal giant cells in the cerebral lesions of tuberous sclerosis complex. Congenital Anomalies. 2007;47.
5. Sampson JR, Scahill SJ, Stephenson JB, Mann L, Connor JM. Genetic aspects of tuberous sclerosis in the west of Scotland. J Med Genet. 1989;26(1):28-31.
6. O'Callaghan FJ, Shiell AW, Osborne JP, Martyn CN. Prevalence of tuberous sclerosis estimated by capture-recapture analysis. Lancet. 1998;351(9114):1490.
7. Ostrom QT, Patil N, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS. CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2013-2017. Neuro Oncol. 2020;22(12 Suppl 2):iv1-iv96.
8. Cardis MA, DeKlotz CMC. Cutaneous manifestations of tuberous sclerosis complex and the paediatrician's role. Arch Dis Child. 2017;102(9):858-63.
9. Northrup H, Aronow ME, Bebin EM, Bissler J, Darling TN, de Vries PJ, et al. Updated International Tuberous Sclerosis Complex Diagnostic Criteria and Surveillance and Management Recommendations. Pediatr Neurol. 2021;123:50-66.
10. Wood MD, Halfpenny AM, Moore SR. Applications of molecular neuro-oncology - a review of diffuse glioma integrated diagnosis and emerging molecular entities. Diagn Pathol. 2019;14(1):29.
11. Barnes A, Wang MM, Feltes J, Ko J, Guzman MA. Subependymal Giant-cell Astrocytoma Masquerading as Restrictive Eating Disorder and Depression in an Adolescent. Innov Clin Neurosci. 2020;17(1-3):10-3.
12. Nguyen HS, Doan NB, Gelsomino M, Shabani S, Awad AJ, Best B, et al. Subependymal Giant Cell Astrocytoma: A Surveillance, Epidemiology, and End Results Program-Based Analysis from 2004 to 2013. World Neurosurg. 2018;118:e263-e8.
13. Krueger DA, Northrup H. Tuberous sclerosis complex surveillance and management: recommendations of the 2012 International Tuberous Sclerosis Complex Consensus Conference. Pediatr Neurol. 2013;49(4):255-65.
14. Jiang T, Jia G, Ma Z, Luo S, Zhang Y. The diagnosis and treatment of subependymal giant cell astrocytoma combined with tuberous sclerosis. Childs Nerv Syst. 2011;27(1):55-62.
15. Tahiri Elousrouti L, Lamchahab M, Bougtoub N, Elfatemi H, Chbani L, Harmouch T, et al. Subependymal giant cell astrocytoma (SEGA): a case report and review of the literature. J Med Case Rep. 2016;10:35.
16. Jung T-Y, Kim Y-H, Jung S, Baek H-J, Lee K-H. The clinical characteristics of subependymal giant cell astrocytoma: five cases. Brain tumor research and treatment. 2015;3(1):44-7.
17. Ekici MA, Kumandas S, Per H, Ekici A, Tucer B, Gumus H, et al. Surgical timing of the subependymal giant cell astrocytoma (SEGA) with the patients of tuberous sclerosis complex. Turk Neurosurg. 2011;21(3):315-24.
18. Ewalt DH, Sheffield E, Sparagana SP, Delgado MR, Roach ES. Renal lesion growth in children with tuberous sclerosis complex. J Urol. 1998;160(1):141-5.
19. Davis PE, Filip-Dhima R, Sideridis G, Peters JM, Au KS, Northrup H, et al. Presentation and Diagnosis of Tuberous Sclerosis Complex in Infants. Pediatrics. 2017;140(6):e20164040.
20. Northrup H, Krueger DA. Tuberous sclerosis complex diagnostic criteria update: recommendations of the 2012 International Tuberous Sclerosis Complex Consensus Conference. Pediatr Neurol. 2013;49(4):243-54.
21. Mongrain V, van Doesburg NH, Rypens F, Fallet-Bianco C, Maassen J, Dufort-Gervais J, et al. A case report of severe tuberous sclerosis complex detected in utero and linked to a novel duplication in the TSC2 gene. BMC Neurol. 2020;20(1):324.
22. Beaumont TL, Godzik J, Dahiya S, Smyth MD. Subependymal giant cell astrocytoma in the absence of tuberous sclerosis complex: case report. J Neurosurg Pediatr. 2015;16(2):134-7.
23. Kim J-Y, Jung T-Y, Lee K-H, Kim S-K. Subependymal Giant Cell Astrocytoma Presenting with Tumoral Bleeding: A Case Report. Brain Tumor Res Treat. 2017;5(1):37-41.
24. Azam M, Rath S, Khurana R, Shukla S, Parween R. Rare case of subependymal giant cell astrocytoma without clinical features of tuberous sclerosis: Case report and literature review. Precision Radiation Oncology. 2017;1(3):108-12.
25. Jacks SK, Witman PM. Tuberous Sclerosis Complex: An Update for Dermatologists. Pediatr Dermatol. 2015;32(5):563-70.
26. Jóźwiak S, Schwartz RA, Janniger CK, Michałowicz R, Chmielik J. Skin lesions in children with tuberous sclerosis complex: their prevalence, natural course, and diagnostic significance. Int J Dermatol. 1998;37(12):911-7.
27. Cascarino M, Leclerc-Mercier S. Histological Patterns of Skin Lesions in Tuberous Sclerosis Complex: A Panorama. Dermatopathology (Basel). 2021;8(3):236-52.
28. Tyburczy ME, Wang J-a, Li S, Thangapazham R, Chekaluk Y, Moss J, et al. Sun exposure causes somatic second-hit mutations and angiofibroma development in tuberous sclerosis complex. Human Molecular Genetics. 2013;23(8):2023-9.
29. Józwiak S, Schwartz RA, Janniger CK, Bielicka-Cymerman J. Usefulness of diagnostic criteria of tuberous sclerosis complex in pediatric patients. J Child Neurol. 2000;15(10):652-9.
30. Fistarol SK, Itin PH. Disorders of pigmentation. J Dtsch Dermatol Ges. 2010;8(3):187-201; quiz -2.
31. Ebrahimi-Fakhari D, Meyer S, Vogt T, Pföhler C, Müller CSL. Dermatological manifestations of tuberous sclerosis complex (TSC). J Dtsch Dermatol Ges. 2017;15(7):695-700.
32. Curatolo P, Bombardieri R, Jozwiak S. Tuberous sclerosis. Lancet. 2008;372(9639):657-68.
33. Muzykewicz DA, Newberry P, Danforth N, Halpern EF, Thiele EA. Psychiatric comorbid conditions in a clinic population of 241 patients with tuberous sclerosis complex. Epilepsy Behav. 2007;11(4):506-13.
34. Goh S, Butler W, Thiele EA. Subependymal giant cell tumors in tuberous sclerosis complex. Neurology. 2004;63(8):1457-61.
35. Nishio S, Morioka T, Suzuki S, Kira R, Mihara F, Fukui M. Subependymal giant cell astrocytoma: clinical and neuroimaging features of four cases. Journal of Clinical Neuroscience. 2001;8(1):31-4.
36. Crino PB, Henske EP. New developments in the neurobiology of the tuberous sclerosis complex. Neurology. 1999;53(7):1384-90.
37. Ironside AJ, Ironside JW. Pathology of tumours of the central nervous system. Surgery (Oxford). 2012;30(3):107-15.
38. Katz JS, Milla SS, Wiggins GC, Devinsky O, Weiner HL, Roth J. Intraventricular lesions in tuberous sclerosis complex: a possible association with the caudate nucleus. Journal of neurosurgery Pediatrics. 2012;9 4:406-13.
39. Gallagher A, Madan N, Stemmer-Rachamimov A, Thiele EA. Progressive calcified tuber in a young male with tuberous sclerosis complex. Dev Med Child Neurol. 2010;52(11):1062-5.
40. Chu-Shore CJ, Frosch MP, Grant PE, Thiele EA. Progressive multifocal cystlike cortical tubers in tuberous sclerosis complex: Clinical and neuropathologic findings. Epilepsia. 2009;50(12):2648-51.
41. Torres OA, Roach ES, Delgado MR, Sparagana SP, Sheffield E, Swift D, et al. Early diagnosis of subependymal giant cell astrocytoma in patients with tuberous sclerosis. J Child Neurol. 1998;13(4):173-7.
42. Dabora SL, Jozwiak S, Franz DN, Roberts PS, Nieto A, Chung J, et al. Mutational Analysis in a Cohort of 224 Tuberous Sclerosis Patients Indicates Increased Severity of TSC2, Compared with TSC1, Disease in Multiple Organs. The American Journal of Human Genetics. 2001;68(1):64-80.
43. Jansen FE, Braams O, Vincken KL, Algra A, Anbeek P, Jennekens-Schinkel A, et al. Overlapping neurologic and cognitive phenotypes in patients with TSC1 or TSC2 mutations. Neurology. 2008;70(12):908-15.
44. Chu-Shore CJ, Major P, Camposano S, Muzykewicz D, Thiele EA. The natural history of epilepsy in tuberous sclerosis complex. Epilepsia. 2010;51(7):1236-41.
45. Yates JR, Maclean C, Higgins JN, Humphrey A, le Maréchal K, Clifford M, et al. The Tuberous Sclerosis 2000 Study: presentation, initial assessments and implications for diagnosis and management. Arch Dis Child. 2011;96(11):1020-5.
46. Jansen FE, Vincken KL, Algra A, Anbeek P, Braams O, Nellist M, et al. Cognitive impairment in tuberous sclerosis complex is a multifactorial condition. Neurology. 2008;70(12):916.
47. Jones AC, Daniells CE, Snell RG, Tachataki M, Idziaszczyk SA, Krawczak M, et al. Molecular genetic and phenotypic analysis reveals differences between TSC1 and TSC2 associated familial and sporadic tuberous sclerosis. Hum Mol Genet. 1997;6(12):2155-61.
48. Józwiak S, Domańska-Pakieła D, Kotulska K, Kaczorowska M. Treatment before seizures: new indications for antiepileptic therapy in children with tuberous sclerosis complex. Epilepsia. 2007;48(8):1632; author reply -4.
49. Humphrey A, Neville BGR, Clarke A, Bolton PF. Autistic regression associated with seizure onset in an infant with tuberous sclerosis. Developmental Medicine & Child Neurology. 2006;48(7):609-11.
50. Bombardieri R, Pinci M, Moavero R, Cerminara C, Curatolo P. Early control of seizures improves long-term outcome in children with tuberous sclerosis complex. European Journal of Paediatric Neurology. 2010;14(2):146-9.
51. Thiele EA. Managing and understanding epilepsy in tuberous sclerosis complex. Epilepsia. 2010;51 Suppl 1:90-1.
52. Vignoli A, La Briola F, Turner K, Peron A, Vannicola C, Chiesa V, et al. Epilepsy in adult patients with tuberous sclerosis complex. Acta Neurol Scand. 2021;144(1):29-40.
53. Ess KC. Tuberous sclerosis complex: a brave new world? Curr Opin Neurol. 2010;23(2):189-93.
54. Specchio N, Pepi C, de Palma L, Moavero R, De Benedictis A, Marras CE, et al. Surgery for drug-resistant tuberous sclerosis complex-associated epilepsy: who, when, and what. Epileptic Disord. 2021;23(1):53-73.
55. Holanda FJCS, Holanda GMP. Tuberous sclerosis — neurosurgical indications in intraventricular tumors. Neurosurgical Review. 1980;3(2):139-50.
56. Turgut M, Akalan N, Özgen T, Ruacan Ş, Erbengi A. Subependymal giant cell astrocytoma associated with tuberous sclerosis: diagnostic and surgical characteristics of five cases with unusual features. Clinical Neurology and Neurosurgery. 1996;98(3):217-21.
57. Kocabaş A, Ekici F, Cetin I, Emir S, Demir HA, Arı ME, et al. Cardiac rhabdomyomas associated with tuberous sclerosis complex in 11 children: presentation to outcome. Pediatr Hematol Oncol. 2013;30(2):71-9.
58. Ghosh S, Milunski MR. Cardiac Rhabdomyoma in Adult. Cureus. 2021;13(4):e14565.
59. Johnson SR, Taveira-DaSilva AM, Moss J. Lymphangioleiomyomatosis. Clin Chest Med. 2016;37(3):389-403.
60. Mizuguchi M. Abnormal giant cells in the cerebral lesions of tuberous sclerosis complex. Congenital Anomalies. 2007;47(1):2-8.
2. Jiang T, Du J, Raynald, Wang J, Li C. Presurgical Administration of mTOR Inhibitors in Patients with Large Subependymal Giant Cell Astrocytoma Associated with Tuberous Sclerosis Complex. World Neurosurg. 2017;107:1053.e1-.e6.
3. Katz JS, Frankel H, Ma T, Zagzag D, Liechty B, Zeev BB, et al. Unique findings of subependymal giant cell astrocytoma within cortical tubers in patients with tuberous sclerosis complex: a histopathological evaluation. Childs Nerv Syst. 2017;33(4):601-7.
4. Mizuguchi M. Abnormal giant cells in the cerebral lesions of tuberous sclerosis complex. Congenital Anomalies. 2007;47.
5. Sampson JR, Scahill SJ, Stephenson JB, Mann L, Connor JM. Genetic aspects of tuberous sclerosis in the west of Scotland. J Med Genet. 1989;26(1):28-31.
6. O'Callaghan FJ, Shiell AW, Osborne JP, Martyn CN. Prevalence of tuberous sclerosis estimated by capture-recapture analysis. Lancet. 1998;351(9114):1490.
7. Ostrom QT, Patil N, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS. CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2013-2017. Neuro Oncol. 2020;22(12 Suppl 2):iv1-iv96.
8. Cardis MA, DeKlotz CMC. Cutaneous manifestations of tuberous sclerosis complex and the paediatrician's role. Arch Dis Child. 2017;102(9):858-63.
9. Northrup H, Aronow ME, Bebin EM, Bissler J, Darling TN, de Vries PJ, et al. Updated International Tuberous Sclerosis Complex Diagnostic Criteria and Surveillance and Management Recommendations. Pediatr Neurol. 2021;123:50-66.
10. Wood MD, Halfpenny AM, Moore SR. Applications of molecular neuro-oncology - a review of diffuse glioma integrated diagnosis and emerging molecular entities. Diagn Pathol. 2019;14(1):29.
11. Barnes A, Wang MM, Feltes J, Ko J, Guzman MA. Subependymal Giant-cell Astrocytoma Masquerading as Restrictive Eating Disorder and Depression in an Adolescent. Innov Clin Neurosci. 2020;17(1-3):10-3.
12. Nguyen HS, Doan NB, Gelsomino M, Shabani S, Awad AJ, Best B, et al. Subependymal Giant Cell Astrocytoma: A Surveillance, Epidemiology, and End Results Program-Based Analysis from 2004 to 2013. World Neurosurg. 2018;118:e263-e8.
13. Krueger DA, Northrup H. Tuberous sclerosis complex surveillance and management: recommendations of the 2012 International Tuberous Sclerosis Complex Consensus Conference. Pediatr Neurol. 2013;49(4):255-65.
14. Jiang T, Jia G, Ma Z, Luo S, Zhang Y. The diagnosis and treatment of subependymal giant cell astrocytoma combined with tuberous sclerosis. Childs Nerv Syst. 2011;27(1):55-62.
15. Tahiri Elousrouti L, Lamchahab M, Bougtoub N, Elfatemi H, Chbani L, Harmouch T, et al. Subependymal giant cell astrocytoma (SEGA): a case report and review of the literature. J Med Case Rep. 2016;10:35.
16. Jung T-Y, Kim Y-H, Jung S, Baek H-J, Lee K-H. The clinical characteristics of subependymal giant cell astrocytoma: five cases. Brain tumor research and treatment. 2015;3(1):44-7.
17. Ekici MA, Kumandas S, Per H, Ekici A, Tucer B, Gumus H, et al. Surgical timing of the subependymal giant cell astrocytoma (SEGA) with the patients of tuberous sclerosis complex. Turk Neurosurg. 2011;21(3):315-24.
18. Ewalt DH, Sheffield E, Sparagana SP, Delgado MR, Roach ES. Renal lesion growth in children with tuberous sclerosis complex. J Urol. 1998;160(1):141-5.
19. Davis PE, Filip-Dhima R, Sideridis G, Peters JM, Au KS, Northrup H, et al. Presentation and Diagnosis of Tuberous Sclerosis Complex in Infants. Pediatrics. 2017;140(6):e20164040.
20. Northrup H, Krueger DA. Tuberous sclerosis complex diagnostic criteria update: recommendations of the 2012 International Tuberous Sclerosis Complex Consensus Conference. Pediatr Neurol. 2013;49(4):243-54.
21. Mongrain V, van Doesburg NH, Rypens F, Fallet-Bianco C, Maassen J, Dufort-Gervais J, et al. A case report of severe tuberous sclerosis complex detected in utero and linked to a novel duplication in the TSC2 gene. BMC Neurol. 2020;20(1):324.
22. Beaumont TL, Godzik J, Dahiya S, Smyth MD. Subependymal giant cell astrocytoma in the absence of tuberous sclerosis complex: case report. J Neurosurg Pediatr. 2015;16(2):134-7.
23. Kim J-Y, Jung T-Y, Lee K-H, Kim S-K. Subependymal Giant Cell Astrocytoma Presenting with Tumoral Bleeding: A Case Report. Brain Tumor Res Treat. 2017;5(1):37-41.
24. Azam M, Rath S, Khurana R, Shukla S, Parween R. Rare case of subependymal giant cell astrocytoma without clinical features of tuberous sclerosis: Case report and literature review. Precision Radiation Oncology. 2017;1(3):108-12.
25. Jacks SK, Witman PM. Tuberous Sclerosis Complex: An Update for Dermatologists. Pediatr Dermatol. 2015;32(5):563-70.
26. Jóźwiak S, Schwartz RA, Janniger CK, Michałowicz R, Chmielik J. Skin lesions in children with tuberous sclerosis complex: their prevalence, natural course, and diagnostic significance. Int J Dermatol. 1998;37(12):911-7.
27. Cascarino M, Leclerc-Mercier S. Histological Patterns of Skin Lesions in Tuberous Sclerosis Complex: A Panorama. Dermatopathology (Basel). 2021;8(3):236-52.
28. Tyburczy ME, Wang J-a, Li S, Thangapazham R, Chekaluk Y, Moss J, et al. Sun exposure causes somatic second-hit mutations and angiofibroma development in tuberous sclerosis complex. Human Molecular Genetics. 2013;23(8):2023-9.
29. Józwiak S, Schwartz RA, Janniger CK, Bielicka-Cymerman J. Usefulness of diagnostic criteria of tuberous sclerosis complex in pediatric patients. J Child Neurol. 2000;15(10):652-9.
30. Fistarol SK, Itin PH. Disorders of pigmentation. J Dtsch Dermatol Ges. 2010;8(3):187-201; quiz -2.
31. Ebrahimi-Fakhari D, Meyer S, Vogt T, Pföhler C, Müller CSL. Dermatological manifestations of tuberous sclerosis complex (TSC). J Dtsch Dermatol Ges. 2017;15(7):695-700.
32. Curatolo P, Bombardieri R, Jozwiak S. Tuberous sclerosis. Lancet. 2008;372(9639):657-68.
33. Muzykewicz DA, Newberry P, Danforth N, Halpern EF, Thiele EA. Psychiatric comorbid conditions in a clinic population of 241 patients with tuberous sclerosis complex. Epilepsy Behav. 2007;11(4):506-13.
34. Goh S, Butler W, Thiele EA. Subependymal giant cell tumors in tuberous sclerosis complex. Neurology. 2004;63(8):1457-61.
35. Nishio S, Morioka T, Suzuki S, Kira R, Mihara F, Fukui M. Subependymal giant cell astrocytoma: clinical and neuroimaging features of four cases. Journal of Clinical Neuroscience. 2001;8(1):31-4.
36. Crino PB, Henske EP. New developments in the neurobiology of the tuberous sclerosis complex. Neurology. 1999;53(7):1384-90.
37. Ironside AJ, Ironside JW. Pathology of tumours of the central nervous system. Surgery (Oxford). 2012;30(3):107-15.
38. Katz JS, Milla SS, Wiggins GC, Devinsky O, Weiner HL, Roth J. Intraventricular lesions in tuberous sclerosis complex: a possible association with the caudate nucleus. Journal of neurosurgery Pediatrics. 2012;9 4:406-13.
39. Gallagher A, Madan N, Stemmer-Rachamimov A, Thiele EA. Progressive calcified tuber in a young male with tuberous sclerosis complex. Dev Med Child Neurol. 2010;52(11):1062-5.
40. Chu-Shore CJ, Frosch MP, Grant PE, Thiele EA. Progressive multifocal cystlike cortical tubers in tuberous sclerosis complex: Clinical and neuropathologic findings. Epilepsia. 2009;50(12):2648-51.
41. Torres OA, Roach ES, Delgado MR, Sparagana SP, Sheffield E, Swift D, et al. Early diagnosis of subependymal giant cell astrocytoma in patients with tuberous sclerosis. J Child Neurol. 1998;13(4):173-7.
42. Dabora SL, Jozwiak S, Franz DN, Roberts PS, Nieto A, Chung J, et al. Mutational Analysis in a Cohort of 224 Tuberous Sclerosis Patients Indicates Increased Severity of TSC2, Compared with TSC1, Disease in Multiple Organs. The American Journal of Human Genetics. 2001;68(1):64-80.
43. Jansen FE, Braams O, Vincken KL, Algra A, Anbeek P, Jennekens-Schinkel A, et al. Overlapping neurologic and cognitive phenotypes in patients with TSC1 or TSC2 mutations. Neurology. 2008;70(12):908-15.
44. Chu-Shore CJ, Major P, Camposano S, Muzykewicz D, Thiele EA. The natural history of epilepsy in tuberous sclerosis complex. Epilepsia. 2010;51(7):1236-41.
45. Yates JR, Maclean C, Higgins JN, Humphrey A, le Maréchal K, Clifford M, et al. The Tuberous Sclerosis 2000 Study: presentation, initial assessments and implications for diagnosis and management. Arch Dis Child. 2011;96(11):1020-5.
46. Jansen FE, Vincken KL, Algra A, Anbeek P, Braams O, Nellist M, et al. Cognitive impairment in tuberous sclerosis complex is a multifactorial condition. Neurology. 2008;70(12):916.
47. Jones AC, Daniells CE, Snell RG, Tachataki M, Idziaszczyk SA, Krawczak M, et al. Molecular genetic and phenotypic analysis reveals differences between TSC1 and TSC2 associated familial and sporadic tuberous sclerosis. Hum Mol Genet. 1997;6(12):2155-61.
48. Józwiak S, Domańska-Pakieła D, Kotulska K, Kaczorowska M. Treatment before seizures: new indications for antiepileptic therapy in children with tuberous sclerosis complex. Epilepsia. 2007;48(8):1632; author reply -4.
49. Humphrey A, Neville BGR, Clarke A, Bolton PF. Autistic regression associated with seizure onset in an infant with tuberous sclerosis. Developmental Medicine & Child Neurology. 2006;48(7):609-11.
50. Bombardieri R, Pinci M, Moavero R, Cerminara C, Curatolo P. Early control of seizures improves long-term outcome in children with tuberous sclerosis complex. European Journal of Paediatric Neurology. 2010;14(2):146-9.
51. Thiele EA. Managing and understanding epilepsy in tuberous sclerosis complex. Epilepsia. 2010;51 Suppl 1:90-1.
52. Vignoli A, La Briola F, Turner K, Peron A, Vannicola C, Chiesa V, et al. Epilepsy in adult patients with tuberous sclerosis complex. Acta Neurol Scand. 2021;144(1):29-40.
53. Ess KC. Tuberous sclerosis complex: a brave new world? Curr Opin Neurol. 2010;23(2):189-93.
54. Specchio N, Pepi C, de Palma L, Moavero R, De Benedictis A, Marras CE, et al. Surgery for drug-resistant tuberous sclerosis complex-associated epilepsy: who, when, and what. Epileptic Disord. 2021;23(1):53-73.
55. Holanda FJCS, Holanda GMP. Tuberous sclerosis — neurosurgical indications in intraventricular tumors. Neurosurgical Review. 1980;3(2):139-50.
56. Turgut M, Akalan N, Özgen T, Ruacan Ş, Erbengi A. Subependymal giant cell astrocytoma associated with tuberous sclerosis: diagnostic and surgical characteristics of five cases with unusual features. Clinical Neurology and Neurosurgery. 1996;98(3):217-21.
57. Kocabaş A, Ekici F, Cetin I, Emir S, Demir HA, Arı ME, et al. Cardiac rhabdomyomas associated with tuberous sclerosis complex in 11 children: presentation to outcome. Pediatr Hematol Oncol. 2013;30(2):71-9.
58. Ghosh S, Milunski MR. Cardiac Rhabdomyoma in Adult. Cureus. 2021;13(4):e14565.
59. Johnson SR, Taveira-DaSilva AM, Moss J. Lymphangioleiomyomatosis. Clin Chest Med. 2016;37(3):389-403.
60. Mizuguchi M. Abnormal giant cells in the cerebral lesions of tuberous sclerosis complex. Congenital Anomalies. 2007;47(1):2-8.
| Files | ||
| Issue | Vol 13 No 4 (2021) | |
| Section | Mini-Reviews | |
| DOI | https://doi.org/10.18502/bccr.v13i4.14402 | |
| Keywords | ||
| Tuberous sclerosis complex Clinic Pathology Mini review | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Darvishi B, Ramezani M. Tuberous sclerosis complex, Clinic and pathology manifestations, Mini -review. Basic Clin Cancer Res. 2022;13(4):284-291.
