Intractable epilepsy in paralimbic Word Health Organization Grade II gliomas: Should the hippocampus be resected when not invaded by the tumor? - Clinical article

Journal of Neurosurgery

Volumn 116, Issue 6, 2012, Pages 1226-1234

  Ghareeb, Fadi ^a   Duffau, Hugues ^b,c  

^a Prince Sultan Military Medical City   (Saudi Arabia)

^b GUI DE CHAULIAC HOSPITAL   (France)

^c MONTPELLIER UNIVERSITY HOSPITAL   (France)

Author keywords

Glioma; Hippocampectomy; Intractable epilepsy; Oncology; Paralimbic tumor; Surgery

Indexed keywords

ADULT; ARTICLE; CANCER GRADING; CANCER INVASION; CANCER SURGERY; CLINICAL ARTICLE; FEMALE; GLIOMA; HIPPOCAMPUS; HUMAN; INTRACTABLE EPILEPSY; LIMBIC CORTEX; MALE; PRIORITY JOURNAL; TREATMENT OUTCOME; WORLD HEALTH ORGANIZATION;

ADULT; EPILEPSY; FEMALE; FOLLOW-UP STUDIES; FRONTAL LOBE; GLIOMA; HIPPOCAMPUS; HUMANS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; LIMBIC SYSTEM; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEUROLOGIC EXAMINATION; POSTOPERATIVE COMPLICATIONS; TEMPORAL LOBE; YOUNG ADULT;

EID: 84861969193     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2012.1.JNS112120     Document Type: Article

References (90)

1. Alonso-Nanclares L, De Felipe J: Vesicular glutamate transporter 1 immunostaining in the normal and epileptic human cerebral cortex. Neuroscience 134:59-68, 2005
2. Amoral LA, Díaz-Guilera A, Moreira AA, Goldberger AL, Lipsitz LA: Emergence of complex dynamics in a simple model of signaling network. Proc Natl Acad Sci U S A 101:15551-15555, 2004
3. Aronica E, Gorter JA, Jansen GH, Leenstra S, Yankaya B, Troost D: Expression of connexin 43 and connexin 32 gapjunction proteins in epilepsy-associated brain tumors and in the perilesional epileptic cortex. Acta Neuropathol 101:449-459, 2001
4. 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 27:223-237, 2001
5. Augustine JR: Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229-244, 1996
6. 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 59:128-138, 2006
7. Bartolomei F, Chauvel P, Wendling F: [Spatio-temporal dynamics of neuronal networks in partial epilepsy.] Rev Neurol (Paris) 161:767-780, 2005 (Fr)
8. Bartolomei F, Wendling F, Bellanger JJ, Régis J, Chauvel P: Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin Neurophysiol 112:1746-1760, 2001
9. Bartolomei F, Wendling F, Régis J, Gavaret M, Guye M, Chauvel P: Pre-ictal synchronicity in limbic networks of mesial temporal lobe epilepsy. Epilepsy Res 61:89-104, 2004
10. Bauer R, Dobesberger J, Unterhofer C, Unterberger I, Walser G, Bauer G, et al: Outcome of adult patients with temporal lobe tumours and medically refractory focal epilepsy. Acta Neurochir (Wien) 149:1211-1217, 2007
11. Blümcke I, Pauli E, Clusmann H, Schramm J, Becker A, Elger C, et al: A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 113:235-244, 2007
12. Brogna C, Gil Robles S, Duffau H: Brain tumors and epilepsy. Expert Rev Neurother 8:941-955, 2008
13. Bromfield EB: Epilepsy in patients with brain tumors and other cancers. Rev Neurol Dis 1 (Suppl 1):S27-S33, 2004
14. Cataltepe O, Turanli G, Yalnizoglu D, Topçu M, Akalan N: Surgical management of temporal lobe tumor-related epilepsy in children. J Neurosurg 102 (3 Suppl):280-287, 2005
15. Chang EF, Potts MB, Keles GE, Lamborn KR, Chang SM, Barbaro NM, et al: Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg 108:227-235, 2008
16. Chavez M, Hwang DU, Amann A, Boccaletti S: Synchronizing weighted complex networks. Chaos 16:015106, 2006
17. Chavez M, Hwang DU, Amann A, Hentschel HG, Boccaletti S: Synchronization is enhanced in weighted complex networks. Phys Rev Lett 94:218701, 2005
18. Craig AD: How do you feel - now? The anterior insula and human awareness. Nat Rev Neurosci 10:59-70, 2009
19. di Michele F, Verdecchia M, Dorofeeva M, Costamagna L, Bernardi G, Curatolo P, et al: GABA(A) receptor active steroids are altered in epilepsy patients with tuberous sclerosis. J Neurol Neurosurg Psychiatry 74:667-670, 2003
20. Duffau H: Contribution of cortical and subcortical electrostimulation in brain glioma surgery: methodological and functional considerations. Neurophysiol Clin 37:373-382, 2007
21. Duffau H: Intraoperative cortico-subcortical stimulations in surgery of low-grade gliomas. Expert Rev Neurother 5:473-485, 2005
22. Duffau H: Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4:476-486, 2005
23. Duffau H: New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity - a review. J Neurooncol 79:77-115, 2006
24. Duffau H: A personal consecutive series of surgically treated 51 cases of insular WHO Grade II glioma: advances and limitations. Clinical article. J Neurosurg 110:696-708, 2009 [Erratum in J Neurosurg 114:1486, 2011]
25. Duffau H: Surgery of low-grade gliomas: towards a 'functional neurooncology'. Curr Opin Oncol 21:543-549, 2009
26. Duffau H, Capelle L: Preferential brain locations of low-grade gliomas. Cancer 100:2622-2626, 2004
27. Duffau H, Capelle L, Lopes M, Bitar A, Sichez JP, van Effenterre R: Medically intractable epilepsy from insular low-grade gliomas: improvement after an extended lesionectomy. Acta Neurochir (Wien) 144:563-573, 2002
28. Duffau H, Capelle L, Lopes M, Faillot T, Sichez JP, Fohanno D: The insular lobe: physiopathological and surgical considerations. Neurosurgery 47:801-811, 2000
29. Duffau H, Gatignol P, Mandonnet E, Capelle L, Taillandier L: Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 109:461-471, 2008
30. Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L: New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128:797-810, 2005
31. Duffau H, Lopes M, Arthuis F, Bitar A, Sichez JP, Van Effenterre R, et al: Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985-96) and with (1996-2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845-851, 2005
32. Duffau H, Moritz-Gasser S, Gatignol P: Functional outcome after language mapping for insular World Health Organization Grade II gliomas in the dominant hemisphere: experience with 24 patients. Neurosurg Focus 27(2):E7, 2009
33. Engel J Jr, Burchfiel J, Ebersole J, Gates J, Gotman J, Homan R, et al: Long-term monitoring for epilepsy. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 87:437-458, 1993
34. Fried I, Kim JH, Spencer DD: Limbic and neocortical gliomas associated with intractable seizures: a distinct clinicopathological group. Neurosurgery 34:815-824, 1994
35. Gil-Robles S, Duffau H: Surgical management of World Health Organization Grade II gliomas in eloquent areas: the necessity of preserving a margin around functional structures. Neurosurg Focus 28(2):E8, 2010
36. Hennessy MJ, Elwes RD, Binnie CD, Polkey CE: Failed surgery for epilepsy. A study of persistence and recurrence of seizures following temporal resection. Brain 123:2445-2466, 2000
37. Hennessy MJ, Elwes RD, Honavar M, Rabe-Hesketh S, Binnie CD, Polkey CE: Predictors of outcome and pathological considerations in the surgical treatment of intractable epilepsy associated with temporal lobe lesions. J Neurol Neurosurg Psychiatry 70:450-458, 2001
38. Herman ST: Epilepsy after brain insult: targeting epileptogenesis. Neurology 59 (9 Suppl 5):S21-S26, 2002
39. Isnard J, Guénot M, Ostrowsky K, Sindou M, Mauguière F: The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 48:614-623, 2000
40. Isnard J, Guénot M, Sindou M, Mauguière F: Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 45:1079-1090, 2004
41. Isnard J, Mauguière F: [The insula in partial epilepsy.] Rev Neurol (Paris) 161:17-26, 2005 (Fr)
42. Jorge CL, Nagahashi-Marie SK, Pedreira CC, Rosemberg S, Valério RM, Valente KD, et al: Clinical characteristics and surgical outcome of patients with temporal lobe tumors and epilepsy. Arq Neuropsiquiatr 58:1002-1008, 2000
43. Jutila L, Immonen A, Mervaala E, Partanen J, Partanen K, Puranen M, et al: Long term outcome of temporal lobe epilepsy surgery: analyses of 140 consecutive patients. J Neurol Neurosurg Psychiatry 73:486-494, 2002
44. Kelly PJ, Daumas-Duport C, Kispert DB, Kall BA, Scheithauer BW, Illig JJ: Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J Neurosurg 66:865-874, 1987
45. Kim OJ, Yong Ahn J, Chung YS, Chung SS, Lee KS, Choi JU, et al: Significance of chronic epilepsy in glial tumors and correlation with surgical strategies. J Clin Neurosci 11:702-705, 2004
46. Klein M, Engelberts NH, van der Ploeg HM, Kasteleijn-Nolst Trenité DG, Aaronson NK, Taphoorn MJ, et al: Epilepsy in low-grade gliomas: the impact on cognitive function and quality of life. Ann Neurol 54:514-520, 2003
47. Lee MC, Kang JY, Seol MB, Kim HS, Woo JY, Lee JS, et al: Clinical features and epileptogenesis of dysembryoplastic neuroepithelial tumor. Childs Nerv Syst 22:1611-1618, 2006
48. Lee MC, Kim GM, Woo YJ, Kim MK, Kim JH, Nam SC, et al: Pathogenic significance of neuronal migration disorders in temporal lobe epilepsy. Hum Pathol 32:643-648, 2001
49. Lombardi D, Marsh R, de Tribolet N: Low grade glioma in intractable epilepsy: lesionectomy versus epilepsy surgery. Acta Neurochir Suppl 68:70-74, 1997
50. Luyken C, Blümcke I, Fimmers R, Urbach H, Elger CE, Wiestler OD, et al: The spectrum of long-term epilepsy-associated tumors: long-term seizure and tumor outcome and neurosurgical aspects. Epilepsia 44:822-830, 2003
51. Lynam LM, Lyons MK, Drazkowski JF, Sirven JI, Noe KH, Zimmerman RS, et al: Frequency of seizures in patients with newly diagnosed brain tumors: a retrospective review. Clin Neurol Neurosurg 109:634-638, 2007
52. Mandonnet E, Pallud J, Clatz O, Taillandier L, Konukoglu E, Duffau H, et al: Computational modeling of the WHO grade II glioma dynamics: principles and applications to management paradigm. Neurosurg Rev 31:263-269, 2008
53. McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, et al: Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery 63:700-708, 2008
54. Morioka T, Hashiguchi K, Nagata S, Miyagi Y, Yoshida F, Shono T, et al: Additional hippocampectomy in the surgical management of intractable temporal lobe epilepsy associated with glioneuronal tumor. Neurol Res 29:807-815, 2007
55. Munari C, Musolino A, Daumas-Duport C, Missir O, Brunet P, Giallonardo AT, et al: Correlation between stereo-EEG, CT-scan and stereotactic biopsy data in epileptic patients with low-grade gliomas. Appl Neurophysiol 48:448-453, 1985
56. Ostrowsky K, Isnard J, Ryvlin P, Guénot M, Fischer C, Mauguière F: Functional mapping of the insular cortex: clinical implication in temporal lobe epilepsy. Epilepsia 41:681-686, 2000
57. Pallud J, Varlet P, Devaux B, Geha S, Badoual M, Deroulers C, et al: Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities. Neurology 74:1724-1731, 2010
58. Panda S, Radhakrishnan VV, Radhakrishnan K, Rao RM, Sarma SP: Electro-clinical characteristics and postoperative outcome of medically refractory tumoral temporal lobe epilepsy. Neurol India 53:66-72, 2005
59. Patt S, Steenbeck J, Hochstetter A, Kraft R, Huonker R, Haueisen J, et al: Source localization and possible causes of interictal epileptic activity in tumor-associated epilepsy. Neurobiol Dis 7:260-269, 2000
60. Perego C, Vanoni C, Bossi M, Massari S, Basudev H, Longhi R, et al: The GLT-1 and GLAST glutamate transporters are expressed on morphologically distinct astrocytes and regulated by neuronal activity in primary hippocampal cocultures. J Neurochem 75:1076-1084, 2000
61. Petrides M, Pandya DN: Efferent association pathways from the rostral prefrontal cortex in the macaque monkey. J Neurosci 27:11573-11586, 2007
62. Phi JH, Kim SK, Cho BK, Lee SY, Park SY, Park SJ, et al: Long-term surgical outcomes of temporal lobe epilepsy associated with low-grade brain tumors. Cancer 115:5771-5779, 2009
63. Plate KH, Wieser HG, Yaşargil MG, Wiestler OD: Neuropathological findings in 224 patients with temporal lobe epilepsy. Acta Neuropathol 86:433-438, 1993
64. Ponten SC, Bartolomei F, Stam CJ: Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 118:918-927, 2007
65. Richardson MP, Hammers A, Brooks DJ, Duncan JS: Benzodiazepine-GABA(A) receptor binding is very low in dysembryoplastic neuroepithelial tumor: a PET study. Epilepsia 42:1327-1334, 2001
66. Riva M: Brain tumoral epilepsy: a review. Neurol Sci 26 (Suppl 1):S40-S42, 2005
67. Rusconi R, Scalmani P, Cassulini RR, Giunti G, Gambardella A, Franceschetti S, et al: Modulatory proteins can rescue a trafficking defective epileptogenic Nav1.1 Na+ channel mutant. J Neurosci 27:11037-11046, 2007
68. Salanova V, Markand O, Worth R: Temporal lobe epilepsy: analysis of patients with dual pathology. Acta Neurol Scand 109:126-131, 2004
69. Sanai N, Berger MS: Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:753-766, 2008
70. Sanai N, Mirzadeh Z, Berger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:18-27, 2008
71. Schaller B: Influences of brain tumor-associated pH changes and hypoxia on epileptogenesis. Acta Neurol Scand 111:75-83, 2005
72. Shaw EG, Berkey B, Coons SW, Bullard D, Brachman D, Buckner JC, et al: Recurrence following neurosurgeon-determined gross-total resection of adult supratentorial low-grade glioma: results of a prospective clinical trial. Clinical article. J Neurosurg 109:835-841, 2008
73. Simon M, Neuloh G, von Lehe M, Meyer B, Schramm J: Insular gliomas: the case for surgical management. Clinical article. J Neurosurg 110:685-695, 2009
74. Smits A, Duffau H: Seizures and the natural history of World Health Organization grade II gliomas: a review. Neurosurgery 68:1326-1333, 2011
75. Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al: Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:1338-1345, 2008
76. Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frénay M, et al: Guidelines on management of low-grade gliomas: report of an EFNS-EANO Task Force. Eur J Neurol 17:1124-1133, 2010
77. Stam CJ, Reijneveld JC: Graph theoretical analysis of complex networks in the brain. Nonlinear Biomed Phys 1:3, 2007
78. Stefan H, Lopes da Silva FH, Löscher W, Schmidt D, Perucca E, Brodie MJ, et al: Epileptogenesis and rational therapeutic strategies. Acta Neurol Scand 113:139-155, 2006
79. Sugano H, Shimizu H, Sunaga S: Efficacy of intraoperative electrocorticography for assessing seizure outcomes in intractable epilepsy patients with temporal-lobe-mass lesions. Seizure 16:120-127, 2007
80. Tang B, Sander T, Craven KB, Hempelmann A, Escayg A: Mutation analysis of the hyperpolarization-activated cyclic nucleotide-gated channels HCN1 and HCN2 in idiopathic generalized epilepsy. Neurobiol Dis 29:59-70, 2008
81. van Breemen MS, Vecht CJ: Optimal seizure management in brain tumor patients. Curr Neurol Neurosci Rep 5:207-213, 2005
82. van Breemen MS, Wilms EB, Vecht CJ: Epilepsy in patients with brain tumours: epidemiology, mechanisms, and management. Lancet Neurol 6:421-430, 2007
83. Wieser HG, Blume WT, Fish D, Goldensohn E, Hufnagel A, King D, et al: ILAE Commission Report. Proposal for a new classification of outcome with respect to epileptic seizures following epilepsy surgery. Epilepsia 42:282-286, 2001
84. Wolf HK, Campos MG, Zentner J, Hufnagel A, Schramm J, Elger CE, et al: Surgical pathology of temporal lobe epilepsy. Experience with 216 cases. J Neuropathol Exp Neurol 52:499-506, 1993
85. Wuttke TV, Lerche H: Novel anticonvulsant drugs targeting voltage-dependent ion channels. Expert Opin Investig Drugs 15:1167-1177, 2006
86. Yaşargil MG: Microneurosurgery. New York: Thieme Medical, Vol 4, 1996
87. Yaşargil MG, Reeves JD: Tumours of the limbic and paralimbic system. Acta Neurochir (Wien) 116:147-149, 1992
88. Yordanova YN, Moritz-Gasser S, Duffau H: Awake surgery for WHO Grade II gliomas within "noneloquent" areas in the left dominant hemisphere: toward a "supratotal" resection. Clinical article. J Neurosurg 115:232-239, 2011
89. Zaatreh MM, Firlik KS, Spencer DD, Spencer SS: Temporal lobe tumoral epilepsy: characteristics and predictors of surgical outcome. Neurology 61:636-641, 2003
90. Zentner J, Meyer B, Stangl A, Schramm J: Intrinsic tumors of the insula: a prospective surgical study of 30 patients. J Neurosurg 85:263-271, 1996