DOI QR코드

DOI QR Code

Factors associated with seizure and cognitive outcomes after epilepsy surgery for low-grade epilepsy-associated neuroepithelial tumors in children

  • Ko, Ara (Division of Pediatric Neurology, Department of Pediatrics, Pusan National University Children's Hospital, Pusan National University College of Medicine) ;
  • Lee, Joon Soo (Division of Pediatric Neurology, Department of Pediatrics, Severance Children's Hospital, Yonsei University College of Medicine)
  • Received : 2019.09.24
  • Accepted : 2019.11.13
  • Published : 2020.05.15

Abstract

Low-grade epilepsy-associated neuroepithelial tumors (LEATs) are responsible for drug-resistant chronic focal epilepsy, and are the second-most common reason for epilepsy surgery in children. LEATs are extremely responsive to surgical treatment, and therefore epilepsy surgery should be considered as a treatment option for LEATs. However, the optimal time for surgery remains controversial, and surgeries are often delayed. In this review, we reviewed published article on the factors associated with seizure and cognitive outcomes after epilepsy surgery for LEATs in children to help clinicians in their decision whether to pursue epilepsy surgery for LEATs. The achievement of gross total resection may be the most important prognostic factor for seizure freedom. A shorter duration of epilepsy, a younger age at surgery, and extended resection of temporal lobe tumors have also been suggested as favorable prognostic factors in terms of seizure control. Poor cognitive function in children with LEATs is associated with a longer duration of epilepsy and a younger age at seizure onset.

Keywords

References

  1. Holthausen H, Blumcke I. Epilepsy-associated tumours: what epileptologists should know about neuropathology, terminology, and classification systems. Epileptic Disord 2016;18:240-51. https://doi.org/10.1684/epd.2016.0851
  2. Bauchet L, Rigau V, Mathieu-Daude H, Fabbro-Peray P, Palenzuela G, Figarella-Branger D, et al. Clinical epidemiology for childhood primary central nervous system tumors. J Neurooncol 2009;92:87-98. https://doi.org/10.1007/s11060-008-9740-0
  3. Koob M, Girard N. Cerebral tumors: specific features in children. Diagn Interv Imaging 2014;95:965-83. https://doi.org/10.1016/j.diii.2014.06.017
  4. Porto L, Jurcoane A, Schwabe D, Hattingen E. Conventional magnetic resonance imaging in the differentiation between high and low-grade brain tumours in paediatric patients. Eur J Paediatr Neurol 2014;18:25-9. https://doi.org/10.1016/j.ejpn.2013.07.004
  5. Forbes JA, Chambless LB, Smith JG, Wushensky CA, Lebow RL, Alvarez J, et al. Use of T2 signal intensity of cerebellar neoplasms in pediatric patients to guide preoperative staging of the neuraxis. J Neurosurg Pediatr 2011;7:165-74. https://doi.org/10.3171/2010.11.PEDS10312
  6. Chen DY, Chen CC, Crawford JR, Wang SG. Tumor-related epilepsy: epidemiology, pathogenesis and management. J Neurooncol 2018;139:13-21. https://doi.org/10.1007/s11060-018-2862-0
  7. van Breemen MS, Wilms EB, Vecht CJ. Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 2007;6:421-30. https://doi.org/10.1016/S1474-4422(07)70103-5
  8. Hildebrand J, Lecaille C, Perennes J, Delattre JY. Epileptic seizures during follow-up of patients treated for primary brain tumors. Neurology 2005;65:212-5. https://doi.org/10.1212/01.wnl.0000168903.09277.8f
  9. Harvey AS, Cross JH, Shinnar S, Mathern GW; ILAE Pediatric Epilepsy Surgery Survey Taskforce. Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia 2008;49:146-55. https://doi.org/10.1111/j.1528-1167.2007.01421.x
  10. Blumcke I, Spreafico R, Haaker G, Coras R, Kobow K, Bien CG, et al. Histopathological findings in brain tissue obtained during epilepsy surgery. N Engl J Med 2017;377:1648-56. https://doi.org/10.1056/NEJMoa1703784
  11. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-30. https://doi.org/10.3322/canjclin.56.2.106
  12. Ullrich NJ, Pomeroy SL, Kapur K, Manley PE, Goumnerova LC, Loddenkemper T. Incidence, risk factors, and longitudinal outcome of seizures in long-term survivors of pediatric brain tumors. Epilepsia 2015;56:1599-604. https://doi.org/10.1111/epi.13112
  13. Chan CH, Bittar RG, Davis GA, Kalnins RM, Fabinyi GC. Long-term seizure outcome following surgery for dysembryoplastic neuroepithelial tumor. J Neurosurg 2006;104:62-9. https://doi.org/10.3171/jns.2006.104.1.62
  14. Giulioni M, Gardella E, Rubboli G, Roncaroli F, Zucchelli M, Bernardi B, et al. Lesionectomy in epileptogenic gangliogliomas: seizure outcome and surgical results. J Clin Neurosci 2006;13:529-35. https://doi.org/10.1016/j.jocn.2005.07.017
  15. Faramand AM, Barnes N, Harrison S, Gunny R, Jacques T, Tahir MZ, et al. Seizure and cognitive outcomes after resection of glioneuronal tumors in children. Epilepsia 2018;59:170-8.
  16. Giulioni M, Marucci G, Pelliccia V, Gozzo F, Barba C, Didato G, et al. Epilepsy surgery of "low grade epilepsy associated neuroepithelial tumors": a retrospective nationwide Italian study. Epilepsia 2017;58: 1832-41. https://doi.org/10.1111/epi.13866
  17. Aronica E, Crino PB. Epilepsy related to developmental tumors and malformations of cortical development. Neurotherapeutics 2014;11:251-68. https://doi.org/10.1007/s13311-013-0251-0
  18. Wolf HK, Birkholz T, Wellmer J, Blumcke I, Pietsch T, Wiestler OD. Neurochemical profile of glioneuronal lesions from patients with pharmacoresistant focal epilepsies. J Neuropathol Exp Neurol 1995;54:689-97. https://doi.org/10.1097/00005072-199509000-00011
  19. Wolf HK, Buslei R, Blumcke I, Wiestler OD, Pietsch T. Neural antigens in oligodendrogliomas and dysembryoplastic neuroepithelial tumors. Acta Neuropathol 1997;94:436-43. https://doi.org/10.1007/s004010050730
  20. Aronica E, Yankaya B, Jansen GH, Leenstra S, van Veelen CW, Gorter JA, et al. Ionotropic and metabotropic glutamate receptor protein expression in glioneuronal tumours from patients with intractable epilepsy. Neuropathol Appl Neurobiol 2001;27:223-37. https://doi.org/10.1046/j.0305-1846.2001.00314.x
  21. Fassunke J, Majores M, Tresch A, Niehusmann P, Grote A, Schoch S, et al. Array analysis of epilepsy-associated gangliogliomas reveals expression patterns related to aberrant development of neuronal precursors. Brain 2008;131(Pt 11):3034-50. https://doi.org/10.1093/brain/awn233
  22. Aronica E, Boer K, Redeker S, Spliet WG, van Rijen PC, Troost D, et al. Differential expression patterns of chloride transporters, Na+-K+- 2Cl--cotransporter and K+-Cl--cotransporter, in epilepsy-associated malformations of cortical development. Neuroscience 2007;145:185-96. https://doi.org/10.1016/j.neuroscience.2006.11.041
  23. Zaghloul KA, Schramm J. Surgical management of glioneuronal tumors with drug-resistant epilepsy. Acta Neurochir (Wien) 2011;153:1551-9. https://doi.org/10.1007/s00701-011-1050-1
  24. Seifert G, Carmignoto G, Steinhauser C. Astrocyte dysfunction in epilepsy. Brain Res Rev 2010;63:212-21. https://doi.org/10.1016/j.brainresrev.2009.10.004
  25. Ye ZC, Rothstein JD, Sontheimer H. Compromised glutamate transport in human glioma cells: reduction-mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange. J Neurosci 1999;19:10767-77. https://doi.org/10.1523/jneurosci.19-24-10767.1999
  26. Aronica E, Gorter JA, Redeker S, Ramkema M, Spliet WG, van Rijen PC, et al. Distribution, characterization and clinical significance of microglia in glioneuronal tumours from patients with chronic intractable epilepsy. Neuropathol Appl Neurobiol 2005;31:280-91. https://doi.org/10.1111/j.1365-2990.2004.00636.x
  27. Prabowo AS, Iyer AM, Anink JJ, Spliet WG, van Rijen PC, Aronica E. Differential expression of major histocompatibility complex class I in developmental glioneuronal lesions. J Neuroinflammation 2013;10:12.
  28. Vezzani A, French J, Bartfai T, Baram TZ. The role of inflammation in epilepsy. Nat Rev Neurol 2011;7:31-40. https://doi.org/10.1038/nrneurol.2010.178
  29. Boer K, Troost D, Timmermans W, van Rijen PC, Spliet WG, Aronica E. Pi3K-mTOR signaling and AMOG expression in epilepsy-associated glioneuronal tumors. Brain Pathol 2010;20:234-44. https://doi.org/10.1111/j.1750-3639.2009.00268.x
  30. Rajneesh KF, Binder DK. Tumor-associated epilepsy. Neurosurg Focus 2009;27:E4. https://doi.org/10.3171/2009.5.FOCUS09101
  31. Ruda R, Trevisan E, Soffietti R. Epilepsy and brain tumors. Curr Opin Oncol 2010;22:611-20. https://doi.org/10.1097/CCO.0b013e32833de99d
  32. Bartolomei F, Bosma I, Klein M, Baayen JC, Reijneveld JC, Postma TJ, et al. How do brain tumors alter functional connectivity? A magnetoencephalography study. Ann Neurol 2006;59:128-38. https://doi.org/10.1002/ana.20710
  33. Steinhauser C, Seifert G. Glial membrane channels and receptors in epilepsy: impact for generation and spread of seizure activity. Eur J Pharmacol 2002;447:227-37. https://doi.org/10.1016/S0014-2999(02)01846-0
  34. Aronica E, Gorter JA, Jansen GH, Leenstra S, Yankaya B, Troost D. Expression of connexin 43 and connexin 32 gap-junction proteins in epilepsy-associated brain tumors and in the perilesional epileptic cortex. Acta Neuropathol 2001;101:449-59. https://doi.org/10.1007/s004010000305
  35. Schmitz AK, Grote A, Raabe A, Urbach H, Friedman A, von Lehe M, et al. Albumin storage in neoplastic astroglial elements of gangliogliomas. Seizure 2013;22:144-50. https://doi.org/10.1016/j.seizure.2012.10.014
  36. Alkonyi B, Mittal S, Zitron I, Chugani DC, Kupsky WJ, Muzik O, et al. Increased tryptophan transport in epileptogenic dysembryoplastic neuroepithelial tumors. J Neurooncol 2012;107:365-72. https://doi.org/10.1007/s11060-011-0750-y
  37. Calatozzolo C, Pollo B, Botturi A, Dinapoli L, Carosi M, Salmaggi A, et al. Multidrug resistance proteins expression in glioma patients with epilepsy. J Neurooncol 2012;110:129-35. https://doi.org/10.1007/s11060-012-0946-9
  38. You G, Sha Z, Jiang T. The pathogenesis of tumor-related epilepsy and its implications for clinical treatment. Seizure 2012;21:153-9. https://doi.org/10.1016/j.seizure.2011.12.016
  39. Shamji MF, Fric-Shamji EC, Benoit BG. Brain tumors and epilepsy: pathophysiology of peritumoral changes. Neurosurg Rev 2009;32:275-84. https://doi.org/10.1007/s10143-009-0191-7
  40. Berntsson SG, Malmer B, Bondy ML, Qu M, Smits A. Tumor-associated epilepsy and glioma: are there common genetic pathways? Acta Oncol 2009;48:955-63. https://doi.org/10.1080/02841860903104145
  41. Ranger A, Diosy D. Seizures in children with dysembryoplastic neuroepithelial tumors of the brain--A review of surgical outcomes across several studies. Childs Nerv Syst 2015;31:847-55. https://doi.org/10.1007/s00381-015-2675-9
  42. Lee JW, Wen PY, Hurwitz S, Black P, Kesari S, Drappatz J, et al. Morphological characteristics of brain tumors causing seizures. Arch Neurol 2010;67:336-42. https://doi.org/10.1001/archneurol.2010.2
  43. Babini M, Giulioni M, Galassi E, Marucci G, Martinoni M, Rubboli G, et al. Seizure outcome of surgical treatment of focal epilepsy associated with low-grade tumors in children. J Neurosurg Pediatr 2013;11:214-23. https://doi.org/10.3171/2012.11.PEDS12137
  44. Daszkiewicz P, Kowalczyk P, Roszkowski M. Surgical treatment of neuronal-glial tumors of mesial-basal part of temporal lobe: Long term outcome and control of epilepsy in pediatric patients. Neurol Neurochir Pol 2018;52:2-8. https://doi.org/10.1016/j.pjnns.2017.04.001
  45. Packer RJ, Sutton LN, Patel KM, Duhaime AC, Schiff S, Weinstein SR, et al. Seizure control following tumor surgery for childhood cortical lowgrade gliomas. J Neurosurg 1994;80:998-1003. https://doi.org/10.3171/jns.1994.80.6.0998
  46. Khajavi K, Comair YG, Wyllie E, Palmer J, Morris HH, Hahn JF. Surgical management of pediatric tumor-associated epilepsy. J Child Neurol 1999;14:15-25. https://doi.org/10.1177/088307389901400102
  47. Brahimaj B, Greiner HM, Leach JL, Horn PS, Stevenson CB, Miles L, et al. The surgical management of pediatric brain tumors causing epilepsy: consideration of the epileptogenic zone. Childs Nerv Syst 2014;30:1383-91. https://doi.org/10.1007/s00381-014-2427-2
  48. Minkin K, Klein O, Mancini J, Lena G. Surgical strategies and seizure control in pediatric patients with dysembryoplastic neuroepithelial tumors: a single-institution experience. J Neurosurg Pediatr 2008;1:206-10. https://doi.org/10.3171/PED/2008/1/3/206
  49. Uliel-Sibony S, Kramer U, Fried I, Fattal-Valevski A, Constantini S. Pediatric temporal low-grade glial tumors: epilepsy outcome following resection in 48 children. Childs Nerv Syst 2011;27:1413-8. https://doi.org/10.1007/s00381-011-1454-5
  50. Yang J, Kim SK, Kim KJ, Chae JH, Lim BC, Wang KC, et al. Satellite lesions of DNET: implications for seizure and tumor control after resection. J Neurooncol 2019;143:437-45. https://doi.org/10.1007/s11060-019-03174-3
  51. Ehrstedt C, Moreira NC, Casar-Borota O, Stromberg B, Ahlsten G. Glioneuronal tumors in childhood - Before and after surgery. A long-term follow-up study. Epilepsy Behav 2017;72:82-8. https://doi.org/10.1016/j.yebeh.2017.02.012
  52. Garcia-Fernandez M, Fournier-Del Castillo C, Ugalde-Canitrot A, Perez-Jimenez A, Alvarez-Linera J, De Prada-Vicente I, et al. Epilepsy surgery in children with developmental tumours. Seizure 2011;20:616-27. https://doi.org/10.1016/j.seizure.2011.06.003
  53. Khajavi K, Comair YG, Prayson RA, Wyllie E, Palmer J, Estes ML, et al. Childhood ganglioglioma and medically intractable epilepsy. A clinicopathological study of 15 patients and a review of the literature. Pediatr Neurosurg 1995;22:181-8. https://doi.org/10.1159/000120899
  54. Ko A, Kim SH, Kim SH, Park EK, Shim KW, Kang HC, et al. Epilepsy surgery for children with low-grade epilepsy-associated tumors: factors associated with seizure recurrence and cognitive function. Pediatr Neurol 2019;91:50-6. https://doi.org/10.1016/j.pediatrneurol.2018.10.008
  55. Ramantani G, Kadish NE, Anastasopoulos C, Brandt A, Wagner K, Strobl K, et al. Epilepsy surgery for glioneuronal tumors in childhood: avoid loss of time. Neurosurgery 2014;74:648-57. https://doi.org/10.1227/NEU.0000000000000327
  56. Englot DJ, Berger MS, Barbaro NM, Chang EF. Factors associated with seizure freedom in the surgical resection of glioneuronal tumors. Epilepsia 2012;53:51-7. https://doi.org/10.1111/j.1528-1167.2011.03269.x
  57. Englot DJ, Berger MS, Barbaro NM, Chang EF. Predictors of seizure freedom after resection of supratentorial low-grade gliomas. A review. J Neurosurg 2011;115:240-4. https://doi.org/10.3171/2011.3.JNS1153
  58. Southwell DG, Garcia PA, Berger MS, Barbaro NM, Chang EF. Longterm seizure control outcomes after resection of gangliogliomas. Neurosurgery 2012;70:1406-13. https://doi.org/10.1227/NEU.0b013e3182500a4c
  59. Kirkpatrick PJ, Honavar M, Janota I, Polkey CE. Control of temporal lobe epilepsy following en bloc resection of low-grade tumors. J Neurosurg 1993;78:19-25. https://doi.org/10.3171/jns.1993.78.1.0019
  60. Blumcke I, Wiestler OD. Gangliogliomas: an intriguing tumor entity associated with focal epilepsies. J Neuropathol Exp Neurol 2002;61:575-84. https://doi.org/10.1093/jnen/61.7.575
  61. Yang I, Chang EF, Han SJ, Barry JJ, Fang S, Tihan T, et al. Early surgical intervention in adult patients with ganglioglioma is associated with improved clinical seizure outcomes. J Clin Neurosci 2011;18:29-33. https://doi.org/10.1016/j.jocn.2010.05.002
  62. Blume WT. The progression of epilepsy. Epilepsia 2006;47 Suppl 1:71-8. https://doi.org/10.1111/j.1528-1167.2006.00665.x
  63. Breier JI, Mullani NA, Thomas AB, Wheless JW, Plenger PM, Gould KL, et al. Effects of duration of epilepsy on the uncoupling of metabolism and blood flow in complex partial seizures. Neurology 1997;48:1047-53. https://doi.org/10.1212/WNL.48.4.1047
  64. Ben-Ari Y, Dudek FE. Primary and secondary mechanisms of epileptogenesis in the temporal lobe: there is a before and an after. Epilepsy Curr 2010;10:118-25. https://doi.org/10.1111/j.1535-7511.2010.01376.x
  65. Hauser WA, Lee JR. Do seizures beget seizures? Prog Brain Res 2002;135:215-9. https://doi.org/10.1016/S0079-6123(02)35021-0
  66. Ogiwara H, Nordli DR, DiPatri AJ, Alden TD, Bowman RM, Tomita T. Pediatric epileptogenic gangliogliomas: seizure outcome and surgical results. J Neurosurg Pediatr 2010;5:271-6. https://doi.org/10.3171/2009.10.PEDS09372
  67. Giulioni M, Rubboli G, Marucci G, Martinoni M, Volpi L, Michelucci R, et al. Seizure outcome of epilepsy surgery in focal epilepsies associated with temporomesial glioneuronal tumors: lesionectomy compared with tailored resection. J Neurosurg 2009;111:1275-82. https://doi.org/10.3171/2009.3.JNS08135
  68. Pelliccia V, Deleo F, Gozzo F, Sartori I, Mai R, Cossu M, et al. Early and late epilepsy surgery in focal epilepsies associated with long-term epilepsyassociated tumors. J Neurosurg 2017;127:1147-52. https://doi.org/10.3171/2016.9.jns161176
  69. Cossu M, Fuschillo D, Bramerio M, Galli C, Gozzo F, Pelliccia V, et al. Epilepsy surgery of focal cortical dysplasia-associated tumors. Epilepsia 2013;54 Suppl 9:115-22. https://doi.org/10.1111/epi.12455
  70. Giulioni M, Marucci G, Martinoni M, Volpi L, Riguzzi P, Marliani AF, et al. Seizure outcome in surgically treated drug-resistant mesial temporal lobe epilepsy based on the recent histopathological classifications. J Neurosurg 2013;119:37-47. https://doi.org/10.3171/2013.3.JNS122132
  71. Bonney PA, Glenn CA, Ebeling PA, Conner AK, Boettcher LB, Cameron DM, et al. Seizure freedom rates and prognostic indicators after resection of gangliogliomas: a review. World Neurosurg 2015;84:1988-96. https://doi.org/10.1016/j.wneu.2015.06.044
  72. Nolan MA, Sakuta R, Chuang N, Otsubo H, Rutka JT, Snead OC 3rd, et al. Dysembryoplastic neuroepithelial tumors in childhood: long-term outcome and prognostic features. Neurology 2004;62:2270-6. https://doi.org/10.1212/01.WNL.0000130495.69512.6F
  73. Santos MV, de Oliveira RS, Machado HR. Approach to cortical dysplasia associated with glial and glioneuronal tumors (FCD type IIIb). Childs Nerv Syst 2014;30:1869-74. https://doi.org/10.1007/s00381-014-2519-z
  74. Lombardi D, Marsh R, de Tribolet N. Low grade glioma in intractable epilepsy: lesionectomy versus epilepsy surgery. Acta Neurochir Suppl 1997;68:70-4.
  75. Qiu B, Ou S, Song T, Hu J, You L, Wang Y, et al. Intraoperative electrocorticography-guided microsurgical management for patients with onset of supratentorial neoplasms manifesting as epilepsy: a review of 65 cases. Epileptic Disord 2014;16:175-84. https://doi.org/10.1684/epd.2014.0662
  76. Sugano H, Shimizu H, Sunaga S. Efficacy of intraoperative electrocorticography for assessing seizure outcomes in intractable epilepsy patients with temporal-lobe-mass lesions. Seizure 2007;16:120-7. https://doi.org/10.1016/j.seizure.2006.10.010
  77. O'Leary DS, Lovell MR, Sackellares JC, Berent S, Giordani B, Seidenberg M, et al. Effects of age of onset of partial and generalized seizures on neuropsychological performance in children. J Nerv Ment Dis 1983;171:624-9. https://doi.org/10.1097/00005053-198310000-00006
  78. Vendrame M, Alexopoulos AV, Boyer K, Gregas M, Haut J, Lineweaver T, et al. Longer duration of epilepsy and earlier age at epilepsy onset correlate with impaired cognitive development in infancy. Epilepsy Behav 2009;16:431-5. https://doi.org/10.1016/j.yebeh.2009.08.008

Cited by

  1. Cognitive and behavioral profiles of pediatric surgical candidates with frontal and temporal lobe epilepsy vol.117, 2020, https://doi.org/10.1016/j.yebeh.2021.107808