418
Case Reports / Journal of Clinical Neuroscience 22 (2015) 418–420
[14] Hohlfeld R, Michels M, Heininger K, et al. Azathioprine toxicity during longterm immunosuppression of generalized myasthenia gravis. Neurology 1988;38:258–61. [15] Finelli PF. Primary CNS lymphoma in myasthenic on long-term azathioprine. J Neurooncol 2005;74:91–2. [16] Kleinschmidt-DeMasters BK, Damek DM, Lillehei KO, et al. Epstein Barr virusassociated primary CNS lymphomas in elderly patients on immunosuppressive medications. J Neuropathol Exp Neurol 2008;67:1103–11.
[17] Herrlinger U, Klingel K, Meyermann R, et al. Central nervous system Hodgkin’s lymphoma without systemic manifestation: case report and review of the literature. Acta Neuropathol 2000;99:709–14. [18] Barthelmes L, Thomas KJ, Seale JR. Prostatic involvement of a testicular lymphoma in a patient with myasthenia gravis on long-term azathioprine. Leuk Lymphoma 2002;43:2425–6. [19] Kuks JB, Djojoatmodjo S, Oosterhuis HJ. Azathioprine in myasthenia gravis: observations in 41 patients and a review of literature. Neuromuscul Disord 1991;1:423–31.
http://dx.doi.org/10.1016/j.jocn.2014.08.003
Multicentric hemispheric ganglioglioma in a 20-year-old adult Shirley P. Ma a,⇑, Alpha Tsui b, Andrew H. Kaye c a b c
Department of Neurosurgery, The University of Melbourne, The Royal Melbourne Hospital, Grattan Street, Parkville, VIC 3052, Australia Department of Anatomical Pathology, The University of Melbourne, The Royal Melbourne Hospital, Parkville, VIC, Australia Department of Surgery, The University of Melbourne, The Royal Melbourne Hospital, Parkville, VIC, Australia
a r t i c l e
i n f o
Article history: Received 23 July 2014 Accepted 2 August 2014
Keywords: Hemispheric Magnetic resonance imaging Multicentric ganglioglioma
a b s t r a c t Gangliogliomas are rare primary central nervous system tumours that characteristically contain both neuronal and glial neoplastic components. They usually present as solitary, slow growing tumours that are frequently associated with pharmacologically refractory epilepsy. Multicentric variants of the tumour are exceedingly rare. We report a 20-year-old patient with multiple gangliogliomas located in the right frontal, temporal and occipital lobes. He presented with headache, fatigue and occasional nausea and vomiting. MRI revealed three large, distinct tumours with striking cyst formation. Stereotactic craniotomy and excision of the temporal and occipital tumours confirmed ganglioglioma. The coincidence of three distinct gangliogliomas involving the right frontal, temporal and occipital lobes has not been reported to our knowledge. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction First described by Perkins in 1926, gangliogliomas are rare primary central nervous system (CNS) tumours accounting for 0.5–1.7% of all neuroepithelial tumours [1] and 1.7–7.6% of all paediatric CNS tumours [2,3]. They characteristically contain both neoplastic glial cells (mainly astrocytes in various states of differentiation) and neuronal cells [4–6]. Multicentric variants of ganglioglioma are exceedingly rare. They are usually reported only in tumours with anaplastic glial components and there is a possible association with neurofibromatosis [7,8]. There have only been four patients with multicentric benign ganglioglioma reported in the literature to date [7–10]. We report a patient with multiple discrete hemispheric gangliogliomas with striking cyst formation. This case is noteworthy in several aspects: (1) the coincidence of three distinct gangliogliomas involving the right frontal, temporal and occipital lobes has not been reported; (2) the clinical presentation was atypical as epilepsy was not a feature despite extensive temporal lobe involvement; and (3) the patient did not have neurofibromatosis. 2. Case report This 20-year-old man was admitted to the Department of Neurosurgery at The Royal Melbourne Hospital after investigations into worsening headache revealed three large, distinct, cystic ⇑ Corresponding author. Tel.: +61 401 180 661. E-mail address: [email protected] (S.P. Ma).
tumours in the right cerebral hemisphere. The patient was symptomatic with chronic headache, more frequent in recent months, associated with fatigue and occasional nausea and vomiting. His past medical history was significant for autism spectrum disorder. There were no features or family history of neurofibromatosis. Physical examinations were unremarkable except for early papilloedema. MRI showed three large, well circumscribed cystic lesions all measuring between 4 and 5 cm in their maximum transverse diameters located in the frontal, temporal and occipital lobes of the right cerebral hemisphere (Fig. 1). T2-weighted and fluid attenuated inversion recovery images showed that there was minimal vasogenic oedema surrounding the lesions, mild sulcal effacement and displacement of the right lateral ventricle, but no obstructive hydrocephalus or acute mass effect. An enhancing mural nodular component was noted on each cyst measuring approximately 1.5–2 cm in diameter. The left cerebral hemisphere was unaffected and no infratentorial lesions were identified. 2.1. Operation The patient underwent a right temporo-occipital craniotomy and excision of the temporal and occipital tumours. The occipital tumour was located 2.5 cm below the cortical surface within the posterior angular sulcus. Although radiologically seemingly well demarcated, both tumors were noted to be moderately infiltrative. Complete macroscopic resection of the cystic and nodular components was obtained. The patient had an uncomplicated post-operative recovery. He underwent no additional adjuvant
Case Reports / Journal of Clinical Neuroscience 22 (2015) 418–420
treatment at this stage and remained asymptomatic. Further surgery is planned for the remaining frontal tumour. 2.2. Pathological findings Histological examination of all the specimens showed features of a moderately cellular glial tumour with similar appearances. There were increased numbers of dysmorphic neurons with
419
enlarged nuclei, prominent nucleoli and abnormally clumped Nissl substance. They stained with B-tubulin, synaptophysin and Neu-N. Elsewhere, there were scattered bipolar astrocytes, which showed focal fascicular arrangement. The tumour cells had elongated and hyperchromatic nuclei. There were some Rosenthal fibres and many eosinophilic granular bodies. The features were consistent with ganglioglioma with the glial component being pilocytic astrocytoma (Fig. 2). 3. Discussion
Fig. 1. MRI demonstrating three large, discrete, hemispheric tumours involving the right frontal, temporal and occipital lobes. Minimal mass effect is observed. The cystic components of the tumours are (a) hypodense on axial T1-weighted images, and (b) hyperdense on axial T2-weighted images. (c) Gadolinium enhancing mural nodular component is noted in the occipital tumour on the axial T1-weighted image. (d) Sagittal view of tumours on fluid attenuated inversion recovery imaging.
Ganglioglioma was first described by Perkins in 1926 as a distinct subtype of primary intracranial neoplasm containing both neuronal and glial dysplastic components. Soon after, Courville reported on the first case series of gangliogliomas in 1930 [11]. These tumours are usually low grade (World Health Organization [WHO] grade I or II) and slow growing, with a favourable prognosis. Although gangliogliomas may arise throughout the neuraxis, they have a distinct predilection for the temporal lobe and tend to present as solitary tumours in the supratentorial parenchyma. Seizures (new or a change in a pre-existing seizure pattern) are often the initial presenting symptom and gangliogliomas are found to be one of the most common causes of tumour-related, pharmacologically refractory, epilepsy in young patients in the first three decades of life [12,13]. Radiologically, ganglioglioma may appear as a partially cystic mass with a mural nodule or solid, welldelineated neoplasm with a tendency for calcification. Total resection is the preferred method of treatment with a 10 year survival rate of 85% [14]. The glial component of ganglioglioma determines disease progression and prognosis. Although generally considered a benign tumour, sporadic cases of malignant ganglioglioma have also been documented. Malignant transformation in ganglioglioma generally occurs when the glial component demonstrates distinct anaplastic features, resembling anaplastic astrocytoma or even glioblastoma [4,15,16]. Multicentric variants of ganglioglioma are exceedingly rare and usually reported in malignant tumours. Yamamoto et al. and AlSarraj et al. documented patients with multifocal gangliocytoma with extensive leptomeningeal dissemination in the brain and spinal cord [17,18]. In those cases, focal anaplasia of the astrocytic component was found. In our patient, there were three clearly discrete tumors, and both excised tumours were classified as
Fig. 2. Haematoxylin and eosin stained sections, original magnification 200. (a) Neuronal component of ganglioglioma, arrow pointing to a neoplastic ganglion cell and (b) glial component of ganglioglioma with bipolar astrocytes and arrow pointing to a Rosenthal fibre, resembling a pilocytic astrocytoma.
420
Case Reports / Journal of Clinical Neuroscience 22 (2015) 418–420
Table 1 Previously documented multicentric benign ganglioglioma Year Authors
Age
1999 Paduch et al. [7]
33
2002 Bradley et al. [9] 2006 Vajramani et al. [10]
2007 Lakhdar et al. [8]
Sex
Seizure Location
Male Present Two right temporal lobe solid tumours 10 mm and 3mm in diameter 8 Male Nil Bitemporal periosteum and dural solid tumours 18 Male Nil Multiple heterogeneous tumours involving the optic chiasm, right lateral geniculate body, right optic radiation and left optic tract 26 Female Nil Multiple heterogenous midbrain, thalamic and deep bilateral paraventricular lesions
Histology Ganglioglioma WHO grade II
Ganglioglioma WHO grade I Ganglioglioma
Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References
Ganglioglioma WHO grade I
WHO = World Health Organization.
WHO grade I ganglioglioma, without any signs of anaplasia or leptomeningeal spread. To the best of our knowledge, there have only been four patients with multifocal benign ganglioglioma reported in the literature. These tumours have been found in the temporal lobe, periosteum and dura, the optic pathway and the brainstem [7–10] (Table 1). Histopathology examinations determined that they were all benign gangliogliomas (WHO grade I/II). Medically refractory epilepsy was documented in one case where two small gangliogliomas were found in the right temporal lobe of a 33-year-old man [7]. There was a suggestion of association with neurofibromatosis when multiple café au lait macules were found on the trunk of a 26-year-old woman with multiple brainstem and deep paraventricular gangliogliomas [8]. Some of the previously documented lesions were heterogenous in their constitution, some with discernible cystic components. The co-incidence of three distinct tumours is extremely rare. The striking cystic formation and hemispheric distribution of tumours was also highly unusual. A normal MRI done when our patient was 4 years of age revealed that the ganglioglioma did not develop in the neonatal/early paediatric period. http://dx.doi.org/10.1016/j.jocn.2014.08.003
In this case report, we describe a multicentric hemispheric ganglioglioma associated with striking cyst formation. The clinical course was atypical of temporal ganglioglioma in that epilepsy was never a clinical feature. The prognosis for multiple gangliogliomas is favourable.
[1] Lote K, Stenwing AE, Skullerud K. Prevalence and prognostic significance of epilepsy in patients with gliomas. Eur J Cancer 1998;34:98–102. [2] Giulioni M, Galassi E, Zucchelli M, et al. Seizure outcome of lesionectomy in glioneuronal tumors associated with epilepsy in children. J Neurosurg 2005;102:S288–93. [3] Morris HH, Estes ML, Gilmore R, et al. Chronic intractable epilepsy as the only symptom of primary brain tumor. Epilepsia 1993;34:1038–43. [4] Dash RC, Provenzale JM, McComb RD, et al. Malignant supratentorial ganglioglioma (ganglion cell-giant cell glioblastoma): a case report and review of the literature. Arch Pathol Lab Med 1999;123:342–5. [5] Luyken C, Blumcke I, Fimmers R, et al. Supratentorial gangliogliomas: histopathologic grading and tumor recurrence in 184 patients with a median follow-up of 8 years. Cancer 2004;101:146–55. [6] de Arriba-Villamor CM, Martinez-Mata A, Espinosa-Mogro H, et al. Ganglion cell tumors. Rev Neurol 1998;27:1008–11. [7] Paduch T, Baborie A, Krauss JK. Bifocal temporal ganglioglioma. Neurosurg Rev 1999;22:112–6. [8] Lakhdar F, Laghmari M, Gana R, et al. Multiple intracranial ganglioglioma case report. Neurochirurgie 2008;54:97–100. [9] Bradley JP, Kure K, Kawamoto HK. Bitemporal ganglioglioma: surgical management of an unusual intracranial and extracranial tumour. Plast Reconstr Surg 2003;111:2328–32. [10] Vajramani GV, Dambatta S, Walker M, et al. Multiple gangliogliomas of the optic pathway. Br J Neurosurg 2006;20:428–30. [11] Courville CB. Ganglioglioma tumor of the central nervous system. Review of the literature and report of two cases. Arch Neurol Psychiatry 1930;24: 439–91. [12] Rousseau A, Kujas M, Bergemer-Fouquet AM, et al. Survivin expression in ganglioglioma. J Neurooncol 2006;77:153–9. [13] Silver JM, Rawlings CE 3rd, Rossitch Jr E, et al. Ganglioglioma: a clinical study with long-term follow-up. Surg Neurol 1991;35:261–6. [14] Baussard B, Di Rocco F, Garnett MR, et al. Pediatric infratentorial gangliogliomas: a retrospective series. J Neurosurg 2007;107:286–91. [15] Kurian NI, Nair S, Radhakrishnan VV. Anaplastic ganglioglioma: case report and review of the literature. Br J Neurosurg 1998;12:277–80. [16] Selvanathan SK, Hammouche S, Salminen HJ, et al. Outcome and prognostic features in anaplastic ganglioglioma: analysis of cases from the SEER database. J Neurooncol 2011;105:539–45. [17] Yamamoto T, Komori T, Shibata N, et al. Multifocal neurocytoma/ gangliocytoma with extensive leptomeningeal dissemination in the brain and the spinal cord. Am J Surg Pathol 1996;20:363–70. [18] al-Sarraj ST. Multifocal neurocytoma/ganglioglioma. Am J Surg Pathol 1997;21:258–9.
Case Reports / Journal of Clinical Neuroscience 22 (2015) 418–420
[14] Hohlfeld R, Michels M, Heininger K, et al. Azathioprine toxicity during longterm immunosuppression of generalized myasthenia gravis. Neurology 1988;38:258–61. [15] Finelli PF. Primary CNS lymphoma in myasthenic on long-term azathioprine. J Neurooncol 2005;74:91–2. [16] Kleinschmidt-DeMasters BK, Damek DM, Lillehei KO, et al. Epstein Barr virusassociated primary CNS lymphomas in elderly patients on immunosuppressive medications. J Neuropathol Exp Neurol 2008;67:1103–11.
[17] Herrlinger U, Klingel K, Meyermann R, et al. Central nervous system Hodgkin’s lymphoma without systemic manifestation: case report and review of the literature. Acta Neuropathol 2000;99:709–14. [18] Barthelmes L, Thomas KJ, Seale JR. Prostatic involvement of a testicular lymphoma in a patient with myasthenia gravis on long-term azathioprine. Leuk Lymphoma 2002;43:2425–6. [19] Kuks JB, Djojoatmodjo S, Oosterhuis HJ. Azathioprine in myasthenia gravis: observations in 41 patients and a review of literature. Neuromuscul Disord 1991;1:423–31.
http://dx.doi.org/10.1016/j.jocn.2014.08.003
Multicentric hemispheric ganglioglioma in a 20-year-old adult Shirley P. Ma a,⇑, Alpha Tsui b, Andrew H. Kaye c a b c
Department of Neurosurgery, The University of Melbourne, The Royal Melbourne Hospital, Grattan Street, Parkville, VIC 3052, Australia Department of Anatomical Pathology, The University of Melbourne, The Royal Melbourne Hospital, Parkville, VIC, Australia Department of Surgery, The University of Melbourne, The Royal Melbourne Hospital, Parkville, VIC, Australia
a r t i c l e
i n f o
Article history: Received 23 July 2014 Accepted 2 August 2014
Keywords: Hemispheric Magnetic resonance imaging Multicentric ganglioglioma
a b s t r a c t Gangliogliomas are rare primary central nervous system tumours that characteristically contain both neuronal and glial neoplastic components. They usually present as solitary, slow growing tumours that are frequently associated with pharmacologically refractory epilepsy. Multicentric variants of the tumour are exceedingly rare. We report a 20-year-old patient with multiple gangliogliomas located in the right frontal, temporal and occipital lobes. He presented with headache, fatigue and occasional nausea and vomiting. MRI revealed three large, distinct tumours with striking cyst formation. Stereotactic craniotomy and excision of the temporal and occipital tumours confirmed ganglioglioma. The coincidence of three distinct gangliogliomas involving the right frontal, temporal and occipital lobes has not been reported to our knowledge. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction First described by Perkins in 1926, gangliogliomas are rare primary central nervous system (CNS) tumours accounting for 0.5–1.7% of all neuroepithelial tumours [1] and 1.7–7.6% of all paediatric CNS tumours [2,3]. They characteristically contain both neoplastic glial cells (mainly astrocytes in various states of differentiation) and neuronal cells [4–6]. Multicentric variants of ganglioglioma are exceedingly rare. They are usually reported only in tumours with anaplastic glial components and there is a possible association with neurofibromatosis [7,8]. There have only been four patients with multicentric benign ganglioglioma reported in the literature to date [7–10]. We report a patient with multiple discrete hemispheric gangliogliomas with striking cyst formation. This case is noteworthy in several aspects: (1) the coincidence of three distinct gangliogliomas involving the right frontal, temporal and occipital lobes has not been reported; (2) the clinical presentation was atypical as epilepsy was not a feature despite extensive temporal lobe involvement; and (3) the patient did not have neurofibromatosis. 2. Case report This 20-year-old man was admitted to the Department of Neurosurgery at The Royal Melbourne Hospital after investigations into worsening headache revealed three large, distinct, cystic ⇑ Corresponding author. Tel.: +61 401 180 661. E-mail address: [email protected] (S.P. Ma).
tumours in the right cerebral hemisphere. The patient was symptomatic with chronic headache, more frequent in recent months, associated with fatigue and occasional nausea and vomiting. His past medical history was significant for autism spectrum disorder. There were no features or family history of neurofibromatosis. Physical examinations were unremarkable except for early papilloedema. MRI showed three large, well circumscribed cystic lesions all measuring between 4 and 5 cm in their maximum transverse diameters located in the frontal, temporal and occipital lobes of the right cerebral hemisphere (Fig. 1). T2-weighted and fluid attenuated inversion recovery images showed that there was minimal vasogenic oedema surrounding the lesions, mild sulcal effacement and displacement of the right lateral ventricle, but no obstructive hydrocephalus or acute mass effect. An enhancing mural nodular component was noted on each cyst measuring approximately 1.5–2 cm in diameter. The left cerebral hemisphere was unaffected and no infratentorial lesions were identified. 2.1. Operation The patient underwent a right temporo-occipital craniotomy and excision of the temporal and occipital tumours. The occipital tumour was located 2.5 cm below the cortical surface within the posterior angular sulcus. Although radiologically seemingly well demarcated, both tumors were noted to be moderately infiltrative. Complete macroscopic resection of the cystic and nodular components was obtained. The patient had an uncomplicated post-operative recovery. He underwent no additional adjuvant
Case Reports / Journal of Clinical Neuroscience 22 (2015) 418–420
treatment at this stage and remained asymptomatic. Further surgery is planned for the remaining frontal tumour. 2.2. Pathological findings Histological examination of all the specimens showed features of a moderately cellular glial tumour with similar appearances. There were increased numbers of dysmorphic neurons with
419
enlarged nuclei, prominent nucleoli and abnormally clumped Nissl substance. They stained with B-tubulin, synaptophysin and Neu-N. Elsewhere, there were scattered bipolar astrocytes, which showed focal fascicular arrangement. The tumour cells had elongated and hyperchromatic nuclei. There were some Rosenthal fibres and many eosinophilic granular bodies. The features were consistent with ganglioglioma with the glial component being pilocytic astrocytoma (Fig. 2). 3. Discussion
Fig. 1. MRI demonstrating three large, discrete, hemispheric tumours involving the right frontal, temporal and occipital lobes. Minimal mass effect is observed. The cystic components of the tumours are (a) hypodense on axial T1-weighted images, and (b) hyperdense on axial T2-weighted images. (c) Gadolinium enhancing mural nodular component is noted in the occipital tumour on the axial T1-weighted image. (d) Sagittal view of tumours on fluid attenuated inversion recovery imaging.
Ganglioglioma was first described by Perkins in 1926 as a distinct subtype of primary intracranial neoplasm containing both neuronal and glial dysplastic components. Soon after, Courville reported on the first case series of gangliogliomas in 1930 [11]. These tumours are usually low grade (World Health Organization [WHO] grade I or II) and slow growing, with a favourable prognosis. Although gangliogliomas may arise throughout the neuraxis, they have a distinct predilection for the temporal lobe and tend to present as solitary tumours in the supratentorial parenchyma. Seizures (new or a change in a pre-existing seizure pattern) are often the initial presenting symptom and gangliogliomas are found to be one of the most common causes of tumour-related, pharmacologically refractory, epilepsy in young patients in the first three decades of life [12,13]. Radiologically, ganglioglioma may appear as a partially cystic mass with a mural nodule or solid, welldelineated neoplasm with a tendency for calcification. Total resection is the preferred method of treatment with a 10 year survival rate of 85% [14]. The glial component of ganglioglioma determines disease progression and prognosis. Although generally considered a benign tumour, sporadic cases of malignant ganglioglioma have also been documented. Malignant transformation in ganglioglioma generally occurs when the glial component demonstrates distinct anaplastic features, resembling anaplastic astrocytoma or even glioblastoma [4,15,16]. Multicentric variants of ganglioglioma are exceedingly rare and usually reported in malignant tumours. Yamamoto et al. and AlSarraj et al. documented patients with multifocal gangliocytoma with extensive leptomeningeal dissemination in the brain and spinal cord [17,18]. In those cases, focal anaplasia of the astrocytic component was found. In our patient, there were three clearly discrete tumors, and both excised tumours were classified as
Fig. 2. Haematoxylin and eosin stained sections, original magnification 200. (a) Neuronal component of ganglioglioma, arrow pointing to a neoplastic ganglion cell and (b) glial component of ganglioglioma with bipolar astrocytes and arrow pointing to a Rosenthal fibre, resembling a pilocytic astrocytoma.
420
Case Reports / Journal of Clinical Neuroscience 22 (2015) 418–420
Table 1 Previously documented multicentric benign ganglioglioma Year Authors
Age
1999 Paduch et al. [7]
33
2002 Bradley et al. [9] 2006 Vajramani et al. [10]
2007 Lakhdar et al. [8]
Sex
Seizure Location
Male Present Two right temporal lobe solid tumours 10 mm and 3mm in diameter 8 Male Nil Bitemporal periosteum and dural solid tumours 18 Male Nil Multiple heterogeneous tumours involving the optic chiasm, right lateral geniculate body, right optic radiation and left optic tract 26 Female Nil Multiple heterogenous midbrain, thalamic and deep bilateral paraventricular lesions
Histology Ganglioglioma WHO grade II
Ganglioglioma WHO grade I Ganglioglioma
Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References
Ganglioglioma WHO grade I
WHO = World Health Organization.
WHO grade I ganglioglioma, without any signs of anaplasia or leptomeningeal spread. To the best of our knowledge, there have only been four patients with multifocal benign ganglioglioma reported in the literature. These tumours have been found in the temporal lobe, periosteum and dura, the optic pathway and the brainstem [7–10] (Table 1). Histopathology examinations determined that they were all benign gangliogliomas (WHO grade I/II). Medically refractory epilepsy was documented in one case where two small gangliogliomas were found in the right temporal lobe of a 33-year-old man [7]. There was a suggestion of association with neurofibromatosis when multiple café au lait macules were found on the trunk of a 26-year-old woman with multiple brainstem and deep paraventricular gangliogliomas [8]. Some of the previously documented lesions were heterogenous in their constitution, some with discernible cystic components. The co-incidence of three distinct tumours is extremely rare. The striking cystic formation and hemispheric distribution of tumours was also highly unusual. A normal MRI done when our patient was 4 years of age revealed that the ganglioglioma did not develop in the neonatal/early paediatric period. http://dx.doi.org/10.1016/j.jocn.2014.08.003
In this case report, we describe a multicentric hemispheric ganglioglioma associated with striking cyst formation. The clinical course was atypical of temporal ganglioglioma in that epilepsy was never a clinical feature. The prognosis for multiple gangliogliomas is favourable.
[1] Lote K, Stenwing AE, Skullerud K. Prevalence and prognostic significance of epilepsy in patients with gliomas. Eur J Cancer 1998;34:98–102. [2] Giulioni M, Galassi E, Zucchelli M, et al. Seizure outcome of lesionectomy in glioneuronal tumors associated with epilepsy in children. J Neurosurg 2005;102:S288–93. [3] Morris HH, Estes ML, Gilmore R, et al. Chronic intractable epilepsy as the only symptom of primary brain tumor. Epilepsia 1993;34:1038–43. [4] Dash RC, Provenzale JM, McComb RD, et al. Malignant supratentorial ganglioglioma (ganglion cell-giant cell glioblastoma): a case report and review of the literature. Arch Pathol Lab Med 1999;123:342–5. [5] Luyken C, Blumcke I, Fimmers R, et al. Supratentorial gangliogliomas: histopathologic grading and tumor recurrence in 184 patients with a median follow-up of 8 years. Cancer 2004;101:146–55. [6] de Arriba-Villamor CM, Martinez-Mata A, Espinosa-Mogro H, et al. Ganglion cell tumors. Rev Neurol 1998;27:1008–11. [7] Paduch T, Baborie A, Krauss JK. Bifocal temporal ganglioglioma. Neurosurg Rev 1999;22:112–6. [8] Lakhdar F, Laghmari M, Gana R, et al. Multiple intracranial ganglioglioma case report. Neurochirurgie 2008;54:97–100. [9] Bradley JP, Kure K, Kawamoto HK. Bitemporal ganglioglioma: surgical management of an unusual intracranial and extracranial tumour. Plast Reconstr Surg 2003;111:2328–32. [10] Vajramani GV, Dambatta S, Walker M, et al. Multiple gangliogliomas of the optic pathway. Br J Neurosurg 2006;20:428–30. [11] Courville CB. Ganglioglioma tumor of the central nervous system. Review of the literature and report of two cases. Arch Neurol Psychiatry 1930;24: 439–91. [12] Rousseau A, Kujas M, Bergemer-Fouquet AM, et al. Survivin expression in ganglioglioma. J Neurooncol 2006;77:153–9. [13] Silver JM, Rawlings CE 3rd, Rossitch Jr E, et al. Ganglioglioma: a clinical study with long-term follow-up. Surg Neurol 1991;35:261–6. [14] Baussard B, Di Rocco F, Garnett MR, et al. Pediatric infratentorial gangliogliomas: a retrospective series. J Neurosurg 2007;107:286–91. [15] Kurian NI, Nair S, Radhakrishnan VV. Anaplastic ganglioglioma: case report and review of the literature. Br J Neurosurg 1998;12:277–80. [16] Selvanathan SK, Hammouche S, Salminen HJ, et al. Outcome and prognostic features in anaplastic ganglioglioma: analysis of cases from the SEER database. J Neurooncol 2011;105:539–45. [17] Yamamoto T, Komori T, Shibata N, et al. Multifocal neurocytoma/ gangliocytoma with extensive leptomeningeal dissemination in the brain and the spinal cord. Am J Surg Pathol 1996;20:363–70. [18] al-Sarraj ST. Multifocal neurocytoma/ganglioglioma. Am J Surg Pathol 1997;21:258–9.
