Clinical Neurology and Neurosurgery 115 (2013) 501–506 Contents lists available at SciVerse ScienceDirect Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro Review Glioblastoma with the appearance of arteriovenous malformation: Pitfalls in diagnosis Matthias Gmeiner a,∗ , Michael Sonnberger b , Gabriele Wurm a , Serge Weis c a b c Division of Neurosurgery, Landes-Nervenklinik Wagner-Jauregg, Linz, Austria Division of Neuroradiology, Landes-Nervenklinik Wagner-Jauregg, Linz, Austria Division of Neuropathology, Landes-Nervenklinik Wagner-Jauregg, Linz, Austria a r t i c l e i n f o Article history: Received 29 August 2012 Received in revised form 3 December 2012 Accepted 9 December 2012 Available online 3 January 2013 Keywords: Glioblastoma Vascular malformation a b s t r a c t Objectives: Very few cases of arteriovenous malformations (AVMs) associated with gliomas were reported so far in the literature. Methods: Here, we report a rare case of a glioblastoma with an AVM-like lesion and review the existing literature. Results: We report an unusual case of a 72-year old woman, who presented with a progressive history of aphasia, memory deficit, and headache. Initial MRI imaging was suggestive of a high-grade glioma for which a pterional craniotomy was performed. Intraoperatively, the lesion resembled a vascular malformation. Total extirpation of the lesion was verified by intraoperative MR imaging. Initial histopathological analysis revealed an AVM. Due to the discrepancy between the radiologic and histopathologic findings, the patient was monitored at close intervals. Two month later, multiple lesions were visible on MRI imaging, thus, supporting the diagnosis of malignant glioma. Therefore, after reinvestigating the histopathological sections and cutting the paraffin block in additional serial sections, in only 5% of the section a glioblastoma was discerned which was surrounded by an AVM-like lesion. Conclusion: Gliomas are rarely found in association with AVMs and require accurate diagnostic evaluation and interpretation for adequate therapeutic interventions. © 2012 Elsevier B.V. All rights reserved. Contents 1. 2. 3. 4. 5. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Materials and methods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Case report . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Review of the literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction Very few cases of arteriovenous malformations (AVMs) associated with gliomas were reported so far in the literature. Although several hypotheses have been generated, the pathogenesis of this lesion remains unclear [25]. Here, we report a rare case of a ∗ Corresponding author at: Division of Neurosurgery, Landes-Nervenklinik Wagner-Jauregg, Wagner-Jauregg-Weg 15A-4020, Linz, Austria. Tel.: +431 0505546228453; fax: +431 0505546225904. E-mail address: matthias.gmeiner@gespag.at (M. Gmeiner). 0303-8467/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2012.12.009 501 501 502 502 503 504 506 506 glioblastoma with an AVM-like lesion and review the existing literature. Such uncommon cases require adequate diagnostic evaluation and interpretation to avoid misdiagnosis. The combined appearance of a glioblastoma and an AVM in the same area has been published in three cases [1,3,19]. Therefore, the publication of such unusual cases in the medical literature is highly warranted. 2. Materials and methods Publications for this review were identified by searching the PubMed using following keywords: “glioblastoma AND vascular 502 M. Gmeiner et al. / Clinical Neurology and Neurosurgery 115 (2013) 501–506 Fig. 1. Preoperative MR imaging demonstrating a left temporal lesion with prominent vessels centrally in axial T2 (A) and contrast enhancement in axial T1 with contrast (B). Elevated cerebral blood flow is demonstrated in perfusion MR (C) with an increased choline peak and decreased NAA peak in MR-spectroscopy (D). malformation”, “glioblastoma AND AVM”, “glioblastoma AND AVM-like malformation” or “angioglioma”. Searching period ranged from 1914 to April 2012. Further, we present a own case of a glioblastoma associated with an AVM-like lesion. 3. Results 3.1. Case report A 72 years old female Caucasian presented in our hospital in October 2011 with an eight weeks history of progressive aphasia, memory deficit, and headache. Initial CT-imaging revealed a left-sided temporal mass lesion with perifocal edema. Additional MRI imaging showed a left temporal lesion with prominent vessels located centrally within the lesion on axial T2 scans (Fig. 1A) and contrast enhancement in axial T1 (Fig. 1B). The contrast enhanced area showed elevated cerebral blood flow on perfusion MR scans (Fig. 1C). MR spectroscopy (Fig. 1D) indicated increased choline and decreased choline/N-acetyl aspartate (NAA) ratios, with an increased choline/NAA ratio above five consistent with a highgrade tumor. Thus, no preoperative angiography was performed. EEG analysis was normal. We decided to perform a left pterional Fig. 2. Intraoperative MR imaging demonstrated complete resection of the contrast enhanced lesion, as seen in axial flair (A) and T1 with contrast (B). M. Gmeiner et al. / Clinical Neurology and Neurosurgery 115 (2013) 501–506 503 Fig. 3. Postoperative MR imaging two month postoperatively. At the edges of the operation site recurrent tumor confirmed the diagnosis of glioblastoma multiforme in flair (A) and T1 with contrast (B). craniotomy using neuronavigation and intraoperative MRI imaging. Intraoperatively, the lesion resembled a vascular malformation. Total resection of the lesion was verified by intraoperative MRI imaging (Fig. 2A and B). A representative specimen was sent for histological examination consisting of several pieces of brownish tissue measuring 2 cm × 1 cm × 0.7 cm in size. The histological section showed an accumulation of numerous vessels of various diameters displaying arterial and venous wall differentiation, some areas of old hemorrhage and reactive astrogliosis were also seen. Postoperatively, a CT angiography was performed showing no vascular malformation. Due to the discrepancy between the preoperative radiographic findings and the histological diagnosis we decided to monitor the patient at close intervals. Two month later, MRI imaging was performed and at the edges of the operation site recurrent tumor was indicative of glioblastoma multiforme on FLAIR-scans (Fig. 3A) and contrast enhanced T1-scans (Fig. 3B). Therefore, histological sections were reinvestigated (Fig. 4) and the paraffin block was cut into additional serial sections (Fig. 5). One area of the section showed a tissue compatible with glioblastoma, i.e. accumulation of astrocytic tumor cells with pleomorphic nuclei and moderate to abundant cytoplasm. These cells stained immunohistochemically positive for GFAP. A moderate number of cells showed signs of proliferation (Ki-67-positive cells). Also a moderate number of cells were immunopositive for p53. The IDH1 R132H mutation could not be demonstrated by immunohistochemistry. However, this tumor area made up only 5% of the whole section. Concomitant radio-chemotherapy was initiated and this patient died in October 2012. 3.2. Review of the literature Vascular malformations associated with gliomas are very rare and include venous malformations, cavernous angioma or arteriovenous malformations. Some authors suggested a separate consideration for these highly vascularized tumors and named them “angiogliomas” [2,4,5,9,10,13,16,24]. Historically, the term angioglioma was first introduced by Councilman [5] who described a highly vascularized cerebellar tumor, that is now regarded as the cellular variant of hemangioblastoma [20]. Whereas Bonnin restricted this term for the combination of glioma and capillary hemangioblastoma [2], Lombardi used the designation for AVMlike vascularized low-grade gliomas. Thus, they reported that from 83 oligodendrogliomas and 155 cerebellar-type or supratentoriell pilocytic astrocytomas 15 cases were diagnosed as angiogliomas. Interestingly, the clinical prognosis of these vascularized low-grade tumors did not differ from those unassociated with hypervascularity [20]. Other authors regard low-grade gliomas associated with any kind of vascular malformation as angiogliomas [10,16], including AVM-like lesions [20], cavernous angiomas [10], and capillary hemangioblastomas [2] (Table 1). Coexistence of AVM and glioma remains a rare event documented only by a few case reports which are summarized in Table 2. Table 1 List of reported “angiogliomas” in the literature. Vascular malformation and tumor within the same location. Author Cases Vascular malformation Tumor histology Lombardi 1991 [20] Lombardi 1991 [20] Lombardi 1991 [20] Hasegawa 1995 [13] Fischer 1982 [9] Fischer 1982 [9] Chee 1985 [4] Gazzeri 2011 [10] Gazzeri 2011 [10] Palma 1995 [29] Bonnin 1983 [2] Bonnin 1983 [2] 4 5 6 1 1 1 1 1 1 2 1 1 AVM-like AVM-like AVM-like Cavernous angioma Cavernous hemangioma Cavernous hemangioma Cavernous angioma Cavernous angioma Cavernous angioma Cavernous angioma Hemangioblastoma Hemangioblastoma Bonnin 1983 [2] Matyja 2007 [24] Kasantikul 1996 [16] Kasantikul 1996 [16] Kasantikul 1996 [16] 1 1 6 3 1 Hemangioblastoma Hemangioblastoma-like Arteriovenous, capillaries, cavernous Arteriovenous, capillaries Cavernous, capillaries Oligodendroglioma Cerebellar-type pilocytic astrocytoma Supratentoriellpilocytic astrocytoma Astrocytoma Oligodendroglioma Glial neoplasia Oligodendroglioma Ganglioglioma Oligodendroglioma Oligodendroglioma Anaplastic astrocytoma Mixed glioma-oligodendrogliomaastroytoma-ependymoma Reactive peripheral astrocytoma Pilocytic astrocytoma Astrocytoma Mixed oligodendroglioma-astrocytoma Oligodendroglioma 504 M. Gmeiner et al. / Clinical Neurology and Neurosurgery 115 (2013) 501–506 Fig. 4. Histomicrographs of the lesion. Scan of the histological section (A). The encircled region shows the area with the suspicious tumor (A and B). (B) The area with the suspicious tumor (H&E stain, magnification 2.5×). (C) Prominent vessel (asterix) with suspicious tumor area (arrow) (H&E stain, magnification 10×). (D) GFAP-positive cells (magnification 20×). (E) Low number of proliferating cells (immunohistochemistry for Ki67, magnification 10×). (F)–(H) Examples of vascular changes consistent with AVM-like lesion (H&E stain, magnification 10×). Thus, 18 cases were reported so far, where an AVM was associated with a glioma and included 7 astrocytomas, 4 oligodendrogliomas, 3 glioblastomas, 2 xanthoastrocytomas, 1 high-grade glioma and 1 gliosarcoma. 4. Discussion We report the case of a 72 year old woman with the histopathological diagnosis of a glioblastoma associated with an AVM-like lesion. Coexistence of AVM and glioma remains a rare event documented only by a few case reports which are summarized in Table 2. Based on the available literature, several hypotheses have been generated: fortuitous separate association [8,14,15,19,23,28,32], combined or sequential lesions [1,3,6,11,12,18,19,22,25,33,34], and a viral origin [9]. Some case reports have documented the coexistence of separately located but not combined or intermixed lesions [8,14,19,23,28,32] that might represent a fortuitous association. Furthermore, an AVM and a glioma might be combined presenting as one lesion [1,3,6,12,18,22,25,33,34]. In some cases, preoperative imaging only revealed one lesion whereas intraoperatively and histopathologically the other lesion could be detected [3,6,33]. In a patient with intracranial hemorrhage, an AVM malformation was diagnosed using cerebral angiography; histopathological analysis revealed a glioblastoma [3]. In two cases, preoperative imaging suggested a tumor mass whereas intraoperatively the associated AVM was observed [6,33]. Harris et al. report one case of development of an AVM, documented on serial angiograms, in the setting of a high-grade astrocytoma. The hyperangiogenic stimulus provided by the tumor might have initiated M. Gmeiner et al. / Clinical Neurology and Neurosurgery 115 (2013) 501–506 505 Fig. 5. The tumor after cutting serial sections. (A) Area displaying the tumor (arrows) and necrosis (asterix) (H&E stain, magnification 5×). (B) Higher magnification of the region displayed in (A) displaying the tumor (arrows) and necrosis (asterix) (H&E stain, magnification 20×). (C) GFAP-positive tumor cells (magnification 20×). (D) Proliferating tumor cells (immunohistochemistry for Ki67, magnification 20×). (E) p53 immunopositive cells (magnification 10×). (F) The tumor does not show the IDH1 R132H mutation (magnification 10×). the development of the AVM [12]. Similarly, McKinney et al. provide evidence about the de novo formation of an AVM within an anaplastic oligodendroglioma in a patient with initially negative brain MR and intracranial MR angiography. The subsequent occurrence of a glioma after the diagnosis of an AVM has even been documented [11,18,19]. Goodkin reports a case, where initially an AVM using cerebral angiography was diagnosed. This lesion regressed and finally disappeared, while in the same period a hypovascular Table 2 AVM and gliomas separate topographical coexistence (sep), AVM and glioma combined in the same location (comb), subsequent occurrence (sequ) of both lesions. Case Author Age/sex Type Tumor histology Radiographic study 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 Fine 1960 [8] Welcker 1966 [32] Heffner 1971 [14] Ho 1981 [15] Licata 1986 [19] Martinez-Lage 1986 [23] Pallud 2009 [28] Crowell 1975 [6] Zuccarello 1979 [34] Malcolm 1991 [22] Harris 2000 [12] Ziyal 2004 [33] McKinney 2008 [25] Cemil 2009 [3] Aucourt 2012 [1] Licata 1986 [19] Lee 1996 [18] Goodkin 1990 [11] 15/m 45/m 17/m 63/f 60/f 43/m 35/m 17/m 50/m 41/m 57/m 58/m 55/f 58/m 65/m 44/m 45/m 9/f Sep Sep Sep Sep Sep Sep Sep Comb Comb Comb Comb Comb Comb Comb Comb Sequ Sequ Sequ Oligodendroglioma Astrocytoma Astrocytoma Astrocytoma Glioblastoma Oligodendroglioma Mal. pleomorphic xanthoastroctoma Oligodendroglioma Mal. astrocytoma Astrocytoma Anaplastic astrocytoma High-grade glioma Anaplastic oligoastrocytoma Glioblastoma Glioblastoma Gliosarcoma Pleomorphic xanthoastrocytoma Anaplastic astrocytoma Ventriculogram angiogram Angiogram Brain scan, angiogram None CT, angiogram CT, angiogram MRI, angiogram Brain scan, angiogram, ventriculogram EEG, angiogram CT, angiogram MRI, angiogram MRI, postop angiogram MRI, angiogram CT, angiogram MRI, angiogram CT, angiogram MRI, CT, angiogram CT, angiogram 506 M. Gmeiner et al. / Clinical Neurology and Neurosurgery 115 (2013) 501–506 mass, histopathologically diagnosed as an anaplastic astrocytoma, developed at the same site. The authors conclude, that the tumor might have stimulated the AVM [11]. These reports provide evidence, that the vascular malformation might have been induced by the tumor. Enhanced angiogenesis, including vessels of increased diameter with high permeability, thickened basement membranes and highly proliferative endothelial cells mediated by proangiogenic factors overexpressed by the tumor is essential for the diagnosis of high-grade gliomas [27]. AVMs are traditionally considered as congenital lesions, although at least seven reports have documented a de novo development. These cases suggest, that inflammatory or ischemic conditions may trigger a de novo AVM [21]. Vascular malformations express a distinct pattern of proangiogenic growth factors [17,31], that are even involved in tumor angiogenesis and vascular homeostasis [27]. One of these, vascular endothelial growth factor, is expressed in both AVM and glioblastomas and other gliomas and therefore, proangiogenic growth factors may be the link between these two pathologies [27]. However, especially in the case of Goodkin, where initially an AVM was diagnosed, it could be speculated that the malformation induced the tumor growth [25]. Similarly, there is evidence in case reports, that an anaplastic oligo-astrocytoma [30] or ependymoma [7] occurs after the resection or at the site of a cerebral cavernous malformation. Nazek reports three cases of nonneoplastic oligodendroglial abnormality in AVMs [26]. Similarly, in 1034 AVMs, although no glioma could be diagnosed 8 cases were found in which oligodendroglial cells were increased [20]. Bonnin supports the hypothesis of reactive astrocytoma in the periphery of a capillary hemangioblastoma due to focal neoplastic transformation of the reactive glial cells [2]. 5. Conclusion In conclusion, we present an unexceptional case of a glioblastoma surrounded by an AVM-like lesion. Whether this is a combined lesion or represents two pathologies remains unclear. If the term angioglioma should be used as a diagnostic term (entity not listed in the WHO classification 2007), both the glioblastoma and the AVM-like lesion should be located in the same topographical region and appear at the same time. However, especially in cases where radiographic, macroscopic and histological findings are inconclusive, accurate histopathological evaluation is required to avoid misdiagnosis and to initiate appropriate treatment strategies. References [1] Aucourt J, Jissendi P, Kerdraon O, Baroncini M. Neuroimaging features and pathology of mixed glioblastoma-AVM complex: a case report. Journal of Neuroradiology. [2] Bonnin JM, Pena CE, Rubinstein LJ. Mixed capillary hemangioblastoma and glioma. A redefinition of the “angioglioma”. Journal of Neuropathology and Experimental Neurology 1983;42:504–16. [3] Cemil B, Tun K, Polat O, Ozen O, Kaptanoglu E. Glioblastoma multiforme mimicking arteriovenous malformation. Turkish Neurosurgery 2009;19: 433–6. [4] Chee CP, Johnston R, Doyle D, Macpherson P. Oligodendroglioma and cerebral cavernous angioma. Case report. Journal of Neurosurgery 1985;62: 145–7. [5] Councilman W. The gliomatous tumors of the brain. Long Island Medical Journal 1914;8:401–9. [6] Crowell RM, DeGirolami U, Sweet WH. Arteriovenous malformation and oligodendroglioma. Case report. Journal of Neurosurgery 1975;43:108–11. [7] Ehtesham M, Kabos P, Yong WH, Schievink WI, Black KL, Yu JS. Development of an intracranial ependymoma at the site of a pre-existing cavernous malformation. Surgical Neurology 2003;60:80–2, discussion 83. [8] Fine RD, Paterson A, Gaylor JB. Recurrent attacks of subarachnoid haemorrhage in presence of a cerebral angioma and an intraventricular oligodendroglioma. Scottish Medical Journal 1960;5:342–5. [9] Fischer EG, Sotrel A, Welch K. Cerebral hemangioma with glial neoplasia (angioglioma?). Report of two cases. Journal of Neurosurgery 1982;56:430–4. [10] Gazzeri R, De Bonis C, Carotenuto V, Catapano D, d’Angelo V, Galarza M. Association between cavernous angioma and cerebral glioma. Report of two cases and literature review of so-called angiogliomas. Neurocirugia (Asturias, Spain) 22:562–566. [11] Goodkin R, Zaias B, Michelsen WJ. Arteriovenous malformation and glioma: coexistent or sequential? Case report. Journal of Neurosurgery 1990;72:798–805. [12] Harris OA, Chang SD, Harris BT, Adler JR. Acquired cerebral arteriovenous malformation induced by an anaplastic astrocytoma: an interesting case. Neurological Research 2000;22:473–7. [13] Hasegawa H, Bitoh S, Koshino K, Obashi J, Kobayashi Y, Kobayashi M, et al. Mixed cavernous angioma and glioma (angioglioma) in the hypothalamus – case report. Neurologia Medico-Chirurgica 1995;35:238–42. [14] Heffner Jr RR, Porro RS, Deck MD. Benign astrocytoma associated with arteriovenous malformation. Case report. Journal of Neurosurgery 1971;35:229–33. [15] Ho KL, Wolfe DE. Concurrence of multiple sclerosis and primary intracranial neoplasms. Cancer 1981;47:2913–9. [16] Kasantikul V, Shuangshoti S, Panichabhongse V, Netsky MG. Combined angioma and glioma (angioglioma). Journal of Surgical Oncology 1996;62:15–21. [17] Kilic T, Pamir MN, Kullu S, Eren F, Ozek MM, Black PM. Expression of structural proteins and angiogenic factors in cerebrovascular anomalies. Neurosurgery 2000;46:1179–91, discussion 1191–1192. [18] Lee TT, Landy HJ, Bruce JH. Arteriovenous malformation associated with pleomorphic xanthoastrocytoma. Acta Neurochirurgica 1996;138:590–1. [19] Licata C, Pasqualin A, Freschini A, Barone G, Da Pian R. Management of associated primary cerebral neoplasms and vascular malformations. 2. Intracranial arterio-venous malformations. Acta Neurochirurgica 1986;83:38–46. [20] Lombardi D, Scheithauer BW, Piepgras D, Meyer FB, Forbes GS. Angioglioma” and the arteriovenous malformation-glioma association. Journal of Neurosurgery 1991;75, 589–566. [21] Mahajan A, Manchandia TC, Gould G, Bulsara KR. De novo arteriovenous malformations: case report and review of the literature. Neurosurgical Review 33:115–119. [22] Malcolm GP, Symon L, Tan LC, Pires M. Astrocytoma and associated arteriovenous malformation. Surgical Neurology 1991;36:59–62. [23] Martinez-Lage JF, Poza M, Esteban JA, Sola J. Subarachnoid hemorrhage in the presence of a cerebral arteriovenous malformation and an intraventricular oligodendroglioma: case report. Neurosurgery 1986;19:125–8. [24] Matyja E, Grajkowska W, Taraszewska A, Marchel A, Bojarski P, Nauman P. Advanced reactive astrogliosis associated with hemangioblastoma versus astroglial-vascular neoplasm (“angioglioma”). Folia Neuropathologica 2007;45:120–5. [25] McKinney JS, Steineke T, Nochlin D, Brisman JL. De novo formation of large arteriovenous shunting and a vascular nidus mimicking an arteriovenous malformation within an anaplastic oligodendroglioma: treatment with embolization and resection. Journal of Neurosurgery 2008;109: 1098–102. [26] Nazek M, Mandybur TI, Kashiwagi S. Oligodendroglial proliferative abnormality associated with arteriovenous malformation: report of three cases with review of the literature. Neurosurgery 1988;23:781–5. [27] Onishi M, Ichikawa T, Kurozumi K, Date I. Angiogenesis and invasion in glioma. Brain Tumor Pathology 28:13–24. [28] Pallud J, Belaid H, Guillevin R, Vallee JN, Capelle L. Management of associated glioma and arteriovenous malformation – the priority is the glioma. British Journal of Neurosurgery 2009;23:197–8. [29] Palma L, Mastronardi L, Celli P, d’Addetta R. Cavernous angioma associated with oligo-astrocytoma-like proliferation. Report of two cases and review of the literature with a reappraisal of the term “angioglioma”. Acta Neurochirurgica 1995;133:169–73. [30] Schreuder T, Te Lintelo M, Kubat B, Koehler P. Anaplastic oligo-astrocytoma occurring after resection of a cerebral cavernous malformation; malignant transformation? Case report and review on etiology. Journal of Neurology 257:349–353. [31] Uranishi R, Baev NI, Ng PY, Kim JH, Awad IA. Expression of endothelial cell angiogenesis receptors in human cerebrovascular malformations. Neurosurgery 2001;48:359–67, discussion 367–358. [32] Welcker ER, Seidel K. Combination of an arteriovenous aneurysmatic angioma with an astrocytoma. Deutsche Zeitschrift fur Nervenheilkunde 1966;189:231–9. [33] Ziyal IM, Ece K, Bilginer B, Tezel GG, Ozcan OE. A glioma with an arteriovenous malformation: an association or a different entity? Acta Neurochirurgica 2004;146:83–6, discussion 86. [34] Zuccarello M, Giordano R, Scanarini M, Mingrino S. Malignant astrocytoma associated with arteriovenous malformation. Case report. Acta Neurochirurgica 1979;50:305–9.