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Neurol Med Chir (Tokyo) 51, 522¿526, 2011

Angiocentric Glioma and Surrounding Cortical Dysplasia Manifesting as Intractable Frontal Lobe Epilepsy —Case Report— Shihomi TAKADA,1 Masaki IWASAKI,2 Hiroyoshi SUZUKI,3 Nobukazu NAKASATO,4 Toshihiro KUMABE,2 and Teiji TOMINAGA2 1Department

of Neurosurgery, Kohnan Hospital, Sendai, Miyagi; Departments of and 4Epileptology, Tohoku University Graduate School of Medicine, Sendai, Miyagi; 3Department of Pathology and Laboratory Medicine, National Hospital Organization Sendai Medical Center, Sendai, Miyagi

2Neurosurgery

Abstract A 26-year-old man presented with a case of angiocentric glioma manifesting as medically refractory epilepsy. Magnetic resonance imaging revealed a hyperintense lesion in the right superior frontal gyrus on T2-weighted imaging, with cortical hyperintense rim on T1-weighted images and minimum contrast enhancement. Video-electroencephalography (EEG) monitoring characterized his seizures as originating from the right frontal lobe. Long-term EEG recording from implanted subdural electrodes disclosed epileptic activities extending beyond the margin of the radiological lesion. Extended cortical resection of the superior frontal gyrus including the tumor and the surrounding epileptic cortices was performed. Postoperatively, he became seizure-free with antiepileptic medication during a 12-month follow-up period. Histological examination of the surgical specimen showed the characteristic findings of angiocentric glioma. Associated cortical dyslamination consistent with cortical dysplasia was found in the surrounding cortex. Angiocentric glioma is a slow-growing or stable tumor frequently presenting with intractable epilepsy. Surgical treatment would be aimed primarily at control of epilepsy. Complete lesionectomy usually results in postoperative seizure freedom, but the present case shows evidence for associated cortical dysplasia with this tumor entity. Careful pre-surgical evaluation for epilepsy is necessary to achieve better seizure outcome. Key words:

angiocentric glioma,

cortical dysplasia,

Introduction

November 2, 2010;

Accepted

intractable epilepsy,

seizure

histological examination revealed cortical dysplasia surrounding the tumor.

Angiocentric glioma was first reported in 2005,4,11) and was recently classified as a new entity in the 2007 World Health Organization Classification of Tumors of the Central Nervous System. Since then, a total of 36 cases have been reported.1–6,8–11) Angiocentric glioma is a slow-growing supratentorial tumor with characteristic radiological features, frequently manifesting as recurrent seizures in children and young adults. Histologically, the tumor is characterized by a perivascular pattern of growth and dotlike staining of microlumens of tumor cells with epithelial membrane antigen (EMA). Angiocentric glioma almost exclusively manifests as medically intractable epilepsy. Presurgical evaluation for epilepsy surgery, not only for tumor removal, is important for the treatment. We treated a patient with angiocentric glioma manifesting as intractable frontal lobe epilepsy whose seizures were controlled after extended lesionectomy. The surgical planning was based on comprehensive evaluation of epilepsy, and the Received

epilepsy surgery,

Case Report A 26-year-old man with intractable complex partial seizures was referred to our hospital for surgical treatment of epilepsy. He had a history of febrile seizures at age 2 years. He had no perinatal problems or family history of epilepsy. He started to have seizures at age 9 years. His seizures were characterized by aura of dizziness and cephalic sensation, followed by loss of awareness, and unintelligible speech and behaviors. Multiple anticonvulsant therapy including carbamazepine, phenytoin, clobazam, gabapentin, and topiramate was administered, but he continued to suffer seizures once a week. Comprehensive pre-surgical evaluation was performed. Magnetic resonance (MR) imaging using whole-body 1.5 and 3.0 Tesla systems (GE Medical Systems, Milwaukee, Wisconsin, USA) revealed an intra-axial tumor of approximately 2 cm diameter with minimum mass effect in the right superior frontal gyrus. The tumor appeared as a

December 16, 2010

522

Angiocentric Glioma and Intractable Epilepsy

Fig. 1 Preoperative magnetic resonance images showing an intra-axial tumor of approximately 2 cm diameter with minimum mass effect in the right superior frontal gyrus (arrow), appearing as a hyperintense lesion of the white matter on T2weighted (D) and fluid-attenuated inversion recovery (FLAIR) images (A, B), rim-like hyperintensity along the cortex on T1weighted images (E, F), and subcortical hypointense area on FLAIR images (A, B). No enhancement with gadolinium was seen (F). Computed tomography scan (C) showed no calcification.

hyperintense lesion of the white matter on T2-weighted and fluid-attenuated inversion recovery (FLAIR) images, rim-like hyperintensity along the cortex on T1-weighted images, and subcortical hypointense area on FLAIR images. No enhancement with gadolinium was seen. Computed tomography showed no calcification (Fig. 1). Long-term video-electroencephalography (EEG) monitoring was performed. A total of 16 seizures including 4 with secondary generalization were captured. Clinically, all episodes were characteristic of his habitual seizures, associated with initial EEG changes in the right frontal region, although the right temporal area was also involved in the later course of the seizure. Interictal epileptic spikes were seen in the right anterior fronto-temporal region. These spikes were mapped in the right anterior frontal lobe using magnetic source imaging. Interictal iodoamphetamine and iomazenil single photon emission computed tomography showed a low uptake area corresponding to the right frontal tumor. Neuropsychological evaluation disclosed mild deficit in general attention, but no material specific dysfunction. Chronic implantation of subdural electrodes was performed to further define the epileptogenic zone and to plan the area of resection. Grid electrodes with 1-cm interelectrode distances (Ad-Tech Medical Instrument Corp., Racine, Wisconsin, USA) were implanted to cover the right lateral and medial frontal lobes. Ictal EEG recordings characterized the onset of seizure as diffuse rhythmic change and background attenuation of the medial frontal leads. Although no focal evolution pattern was observed, fast epileptiform discharges were present around and in the remote region of the tumor. Interictal spikes were distributed over a wide area in the right frontal lobe. The

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Fig. 2 Invasive preoperative evaluation with subdural grid electrodes. The location of electrodes is illustrated. On the ictal electroencephalography recordings, seizure discharges were associated with fast epileptiform activities around and in the remote region of the tumor (stars). Interictal spikes were distributed over a wide area in the right frontal lobe (gray circles), although the most frequent populations (dark gray circles) were located around, but not confined to, the lesion.

Fig. 3 A: Photograph of the surgical specimen of the removed cortex. The medial surface of the superior frontal gyrus is shown. The tumor was only appreciable as slightly pale and yellowish color. The tumor was identified in the dotted area, and cortical dysplasia was found in the adjacent cortex (asterisk). B: Postoperative T2-weighted magnetic resonance images showing the extent of resection and no evidence of residual tumor.

most frequent spike populations were located around, but not confined to, the lesion (Fig. 2). En bloc resection of the right superior frontal gyrus was performed under the guidance of intraoperative electrocorticography recording. The resection included the tumor and the surrounding cortices harboring the ictal

524

S. Takada et al. logical deficits. He remained free from seizures with antiepileptic medications and showed no evidence of tumor recurrence during the 12-month follow-up period. Immunohistochemical examination showed the tumor consisted of spindle-shaped cells positive for glial fibrillary acidic protein and large round-shaped cells with high nuclear-cytoplasm ratio. The spindle-shaped cells were characterized by schwannoma-like palisade arrangement, with orthogonal aggregation to the cortical surface and formation of perivascular rosettes. These cells were positive for vimentin, negative for chromogranin A, and characterized by dot-like structures positive for EMA in the cytoplasm (Fig. 4). There were no mitotic figures. Ki-67 labeling index was 1% throughout the specimen. The immediate surrounding region showed histological characteristics compatible with cortical dysplasia (Fig. 5).

Fig. 4 A, B: Photomicrographs showing the tumor characterized by schwannoma-like palisade arrangement of the spindleshaped cells (A), with orthogonal aggregation to the cortical surface (B) and formation of perivascular rosettes. Hematoxylin and eosin stain, original magnification ×100. C, D: Immunohistochemical staining showing the tumor consisted of spindle-shaped cells positive for glial fibrillary acidic protein (C) and large round-shaped cells with relatively high nuclearcytoplasm ratio. These cells were characterized by dot-like structures positive for epithelial membrane antigen in the cytoplasm (D). Original magnification ×400.

Fig. 5 Photomicrographs showing the adjacent cortex (asterisk in Fig. 3A) characterized by dyslamination of cortical cell layers (A), abnormal aggregation of pyramidal neurons (B, arrow), dysmorphism of cell nucleus (C, arrows), and pericapillary aggregation of oligodendrocyte-like cells (C, arrowhead). Hematoxylin and eosin stain, original magnification A: ×100, B: ×400, C: ×200.

epileptiform discharges and most frequent spikes. Intraoperatively, the surface structure of the brain was generally intact, and the tumor was only appreciable as a slightly pale and yellowish color. Postoperative MR imaging confirmed the absence of residual tumor (Fig. 3). The postoperative course was uneventful without new neuro-

Discussion A total of 37 patients with angiocentric glioma including the present case have been reported (Table 1).1–6,8–11) The defining histological features of this tumor are the striking perivascular pattern of growth, schwannoma-like palisade arrangement of tumor cells, and characteristic ``dot-like'' EMA staining of microlumens of the tumor, suggesting ependymal differentiation in part. The neuroimaging features include solid T2-weighted hyperintense lesion in the superficial cerebrum with no contrast enhancement. Cortical rim-like hyperintensity on T1-weighted images and the stalk-like extension to the ventricle on T2-weighted images were also reported.4,8) All of the above features were consistently found in our case. The majority of the patients (34 of 37 cases) with angiocentric glioma presented with epileptic seizures, almost all intractable to antiepileptic medications (Table 1). The mean age was 11.1 years (range 2–55 years) at the onset of epilepsy and 17.7 years (2–70 years) at surgical treatment. The tumor arose exclusively in the supratentorial cerebrum, frequently in the frontal (36.1%) and temporal (34.7%) lobes, followed by the parietal (22.2%) and occipital (6.9%) lobes. A single case of midbrain tumor with histological features similar to angiocentric glioma was also reported.2) No recurrence or progression has been reported after gross total or subtotal removal of tumor, except for one patient who died of tumor progression 62 months after the first surgery.11) Ki-67 labeling index was 1% or less in 18 of 29 reported cases (62.1%). The tumor has benign nature, so the primary goal of surgical treatment is control of the epileptic seizures. Excellent seizure outcome can be expected if total removal of the tumor is achieved. After more than 12 months follow up in the previous cases,3,4,8,9,11) postoperative seizure freedom was achieved in all 15 cases after gross total removal, but in only 2 of 6 cases after subtotal removal. In the present case, EEG evaluation with implanted subdural electrodes revealed epileptogenic activities over a wider area than the tumor. Removal of the neurophysiological epileptic cortices in addition to the tumor resulted in freedom from seizures after surgery, and disclosed cortical dysplasia in the surrounding cortex.

Neurol Med Chir (Tokyo) 51, July, 2011

Neurol Med Chir (Tokyo) 51, July, 2011

Sugita et al. (2008)10) Lum et al. (2008)5)

Preusser et al. (2007)8)

Lellouch-Tubiana et al. (2005)4)

Wang et al. (2005)11)

Sex

F F M M F F M M F M M F M F F M F M M F M F M M F F M M

Age at operation (yrs)

15

4

3 14 12 30

26

37 5

7 2.3 10.5 6.5 12 14.5

13.5 6.4 15.5 6

9 15 15

17

35 37 70 6

14

DRE

DRE DRE DRE DRE

DRE

DRE DRE DRE refractory status epilepticus DRE DRE DRE

DRE DRE DRE DRE DRE DRE

DRE DRE

DRE

Sz DRE DRE DRE

DRE

Sz

Presenting symptoms

Summary of 37 cases of angiocentric glioma

Author (Year)

Table 1

13

10 childhood 13 5

14

8 3 12

12 3 10 6

6.5 2 4 4.5 9.5 13

19 4

23

3 10 3 5

4

11

Age at onset of epilepsy (yrs)

rt F

P medial T medial T rt O-P

F-P operculum

inferior T P P

lt F-T rt F-P lt medial T rt P lt F rt orbito-F to insula rt P lt F lt F medial T

rt F lt anterior T

lt O rt posterior F rt orbito-F lt anteromedial T lt F

rt P

rt medial T

Location of tumor

GTR

GTR GTR GTR+ radiation biopsy+ radiation STR GTR GTR GTR

GTR STR STR STR

GTR STR GTR GTR GTR STR

STR+radiochemotherapy n.d. GTR

GTR+radiochemotherapy STR GTR STR GTR

GTR

Treatment

n.d.

6 12 83 9

24

56 60 7

24 14 12 57

165 36 72 60 2.3 24

n.d. 168

62

36 24 24 48

48

12

Follow-up period (mos)

free free free free Sz free

Sz Sz Sz Sz

Sz free

Sz free Sz free Sz free

Sz free rare Sz rare Sz Sz free

Sz free rare Sz Sz free Sz free Sz free rare Sz

n.d. n.d.

n.d.

Sz free n.d. n.d. Sz free

Sz free

Sz free

Sz

Tumor

rec. prog. prog. rec.

prog. rec. rec. rec. n.d.

no no no no

no prog.

no rec. no rec. no rec.

no no no no

n.d. no prog. no rec. no rec. no rec. no prog.

n.d. n.d.

prog. (dead)

no prog. no rec. no prog. n.d.

n.d.

no rec.

Outcome

º5%

º1% 2% º1% 8%

3%

º1% 5% º1%

1% 1–2% 1–2% 2%

º1% 2–3% º1% º1% º1% º1%

Contd.

1% (10% at second surgery) 1% 1–2%

1% n.d. 1% n.d.

5%

n.d.

MIB-1 index

Angiocentric Glioma and Intractable Epilepsy 525

midbrain

1% no rec. Sz free 12 GTR

DRE

hydrocephalus

DRE

F

F

M

9 26

5

Fulton et al. (2009)3) Mott et al. (2010)6) Covington et al. (2010)2) Present case

57

53

8 n.d. 2 M F M 10 13 2

headache, decreasing visual acuity DRE DRE DRE M Shakur et al. (2009)9)

10

55 asymptomatic 55

M



rt F

º1%

no prog. no prog. 24

1% regression Sz free 5

biopsy+ radiation STR rt F

n.d. low n.d. no rec. n.d. n.d. lt middle T lt anterior T rt F-P

GTR GTR GTR

9 6 14

Sz free Sz free Sz free

n.d. no rec. —

lt posterior T

GTR

24

negative n.d. rt T

GTR

n.d.

death (unrelated) —

negative n.d. Sz free 2 GTR lt O 10 DRE M 20 Arsene et al. (2008)1)

MIB-1 index Tumor Sz

Outcome Follow-up period (mos) Treatment Location of tumor Age at onset of epilepsy (yrs) Presenting symptoms Sex Age at operation (yrs) Author (Year)

contd. Table 1

DRE: drug-resistant epilepsy, F: frontal, GTR: gross total removal, n.d.: not described, O: occipital, P: parietal, prog.: progression, rec.: recurrence, STR: subtotal removal, Sz: seizure, T: temporal.

S. Takada et al.

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Epileptogenic tumors, such as ganglioglioma and dysembryoplastic neuroepithelial tumor, are known to be associated with adjacent malformation of cortical development.7) This association has not been reported in angiocentric glioma. The present case shows that angiocentric glioma has similar histological consequences as epileptogenic tumors. Epileptogenicity may reside in the dysplastic cortices as well as the tumor. Therefore, lesionectomy including the adjacent cortical dysplasia is necessary in some patients to achieve complete seizure freedom after surgery.

References 1)

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11)

Arsene D, Ardeleanu C, Ogrezeanu I, Danaila L: Angiocentric glioma: presentation of two cases with dissimilar histology. Clin Neuropathol 27: 391–395, 2008 Covington DB, Rosenblum MK, Brathwaite CD, Sandberg DI: Angiocentric glioma-like tumor of the midbrain. Pediatr Neurosurg 45: 429–433, 2010 Fulton SP, Clarke DF, Wheless JW, Ellison DW, Ogg R, Boop FA: Angiocentric glioma-induced seizures in a 2-year-old child. J Child Neurol 24: 852–856, 2009 Lellouch-Tubiana A, Boddaert N, Bourgeois M, Fohlen M, Jouvet A, Delalande O, Seidenwurm D, Brunelle F, SainteRose C: Angiocentric neuroepithelial tumor (ANET): a new epilepsy-related clinicopathological entity with distinctive MRI. Brain Pathol 15: 281–286, 2005 Lum DJ, Halliday W, Watson M, Smith A, Law A: Cortical ependymoma or monomorphous angiocentric glioma? Neuropathology 28: 81–86, 2008 Mott RT, Ellis TL, Geisinger KR: Angiocentric glioma: A case report and review of the literature. Diagn Cytopathol 38: 452–456, 2010 Prayson RA, Estes ML, Morris HH: Coexistence of neoplasia and cortical dysplasia in patients presenting with seizures. Epilepsia 34: 609–615, 1993 Preusser M, Hoischen A, Novak K, Czech T, Prayer D, Hainfellner JA, Baumgartner C, Woermann FG, Tuxhorn IE, Pannek HW, Bergmann M, Radlwimmer B, Villagran R, Weber RG, Hans VH: Angiocentric glioma: report of clinico-pathologic and genetic findings in 8 cases. Am J Surg Pathol 31: 1709–1718, 2007 Shakur SF, McGirt MJ, Johnson MW, Burger PC, Ahn E, Carson BS, Jallo GI: Angiocentric glioma: a case series. J Neurosurg Pediatr 3: 197–202, 2009 Sugita Y, Ono T, Ohshima K, Niino D, Ito M, Toda K, Baba H: Brain surface spindle cell glioma in a patient with medically intractable partial epilepsy: a variant of monomorphous angiocentric glioma? Neuropathology 28: 516–520, 2008 Wang M, Tihan T, Rojiani AM, Bodhireddy SR, Prayson RA, Iacuone JJ, Alles AJ, Donahue DJ, Hessler RB, Kim JH, Haas M, Rosenblum MK, Burger PC: Monomorphous angiocentric glioma: a distinctive epileptogenic neoplasm with features of infiltrating astrocytoma and ependymoma. J Neuropathol Exp Neurol 64: 875–881, 2005

Address reprint requests to: Masaki Iwasaki, MD, Department of Neurosurgery, Tohoku University Graduate School of Medicine, 1–1 Seiryo–machi, Aoba–ku, Sendai, Miyagi 980–8574, Japan. e-mail: epinetmi@gmail.com

Neurol Med Chir (Tokyo) 51, July, 2011