J Neurosurg 72:798-805, 1990 Arteriovenous malformation and glioma: coexistent or sequential? Case report ROBERT GOODKIN, M . D . , BARBARA ZAIAS~ M.D., AND W. JOST MICHELSEN, M.D. Departments of Neurological Surgery and Pathology, City' of tlope National Medical Center, Duarte, California; Department of Neuroh)gical Surgery, University of Southern California School of Medicine, Los Angeles, California; and Department of Neurological Surgery, Neurological Institute of New York, New York, New York u- A 9-year-old girl was evaluated for behavioral changes and seizures. Initial computerized tomography and cerebral angiography revealed a left cerebral vascular mass, diagnosed as an arteriovenous malformation. An embolization procedure was attempted but was terminated before completion because the patient developed a right hemiparesis. Her fight-sided neurological deficit subsequently increased with enlargement of the mass lesion. On follow-up cerebral angiography approximately 2 years later the vascular maltbrmation was no longer demonstrated. Biopsy of the mass lesion revealed it to be an anaplastic astrocytoma. This case is reported with a review of the literature on the coexistence of a brain tumor and a vascular malformation, the difficulties in diagnosis, and possible etiologies. KEY WORDS " arteriovenous malformation R ARELY is there confusion in differentiating a brain t u m o r with a b n o r m a l vasculature from an arteriovenous m a l f o r m a t i o n (AVM) of the brain. This report describes a 9-year-old girl in whom a left cerebral mass lesion, initially diagnosed a n d treated as an AVM, was subsequently proved f r o m biopsy e x a m i n a t i o n to be an astrocytoma. This case raises several questions as to the possible etiology: that is, the coexistence o f two separate lesions, the evolution of one lesion into the other, a single "multipotential" lesion, or misdiagnosis. Case Report This 9-year-old Caucasian girl started to tire easily a n d her face occasionally b e c a m e "beet red" beginning in September, 1983. In N o v e m b e r , 1983, she developed a seizure. A l u m b a r puncture showed clear colorless cerebrospinal fluid (CSF). A computerized tomography (CT) brain scan on N o v e m b e r 15, 1983, showed a contrast-enhancing lesion in the left centrosylvian region, with draining veins into the vein o f Galen and straight sinus (Fig. 1). There was a large low-density area in the left middle fossa consistent with CSF, believed to be a dilated trapped temporal horn of the left 798 9 glioma 9 brain neoplasm lateral ventricle. There was a slight midline shift from left to right. Bilateral cerebral and left vertebral angiography (Fig. 2) performed on N o v e m b e r 16 revealed vascular m a l f o r m a t i o n with some mass effect in the left centrosylvian region, being fed primarily by the left anterior choroidal artery, left lenticulostriate branches of the insular loops of the left middle cerebral artery, left medial a n d lateral choroidal artery, branches o f the left posterior cerebral artery, and (to a lesser extent) the left thalmoperforating artery. Primary drainage was into the vein o f Galen and straight sinus. This constellation of findings was considered compatible with an AVM of the left cerebrum. Anticonvulsant medication was initiated. In January, 1984, follow-up CT revealed a slightly increased left-to-right shift of the midline, but the appearance was otherwise essentially similar to the changes seen in N o v e m b e r , 1983. The patient was referred for embolization of the AVM. T h e procedure was terminated when, during two test balloon inflations, she developed a right hemiparesis. In June, 1984, a fight visual field defect was d e m o n strated. In July, repeat C T without contrast enhancem e n t showed enlargement o f the left cerebral lesion, J. Neurosurg. / Volume 72/May, 1990 AVM and glioma at same cerebral site FIG. 1. Computerized tomography scan with contrast enhancement obtained on November 15, 1983. A contrastenhancing lesion is seen in the left cerebrum. There is a mild left-to-right midline shift. increased left-to-right shift, a n d ventricular enlargement. The patient's right hemiparesis increased. There was no hemiatrophy. The patient was referred for follow-up examination and, on D e c e m b e r 12, 1984, repeat cerebral and posterior fossa angiography revealed a decrease in the vascular c o m p o n e n t o f the mass lesion, occlusion of some feeding vessels, a n d an increase in the left temporal mass effect. At this time the possibility that the mass lesion was an evolving primary brain t u m o r was considered. The patient u n d e r w e n t a left ventriculoperitoneal shunt procedure with placement o f the ventricular end o f the shunt system into the fluid- FIG. 3. Left carotid angiogram, lateral view arterial phase, obtained on September 10, 1985. The previously seen arteriovenous malformation is not visualized on this or on vertebral angiography. filled cavity considered to be a t r a p p e d t e m p o r a l h o r n o f the left lateral ventricle. T h e fluid was x a n t h r o c h r o mic, a n d cytological e x a m i n a t i o n o f the fluid speci m e n revealed n o evidence o f a b n o r m a l cells. After shunt placement, the patient's neurological status transiently i m p r o v e d . A follow-up C T scan s h o w e d d e c o m pression o f the fluid-filled cavity in the left t e m p o r a l lobe a n d decreased midline shift w i t h o u t a change in FIG. 2. Left carotid angiogram, lateral view (left), and left vertebral angiogram, lateral view (right), obtained on November 16, 1983. An arteriovenous malformation is evident in the left cerebrum. J. Neurosurg. / Volume 7 2 / M a y , 1990 799 R. Goodkin, the left cerebral mass lesion; however, serial follow-up C T scans demonstrated progressive enlargement of the left cerebral mass lesion. In August, 1985, it had b e c o m e apparent to the parents that the patient's condition was deteriorating, primarily manifested by withdrawal from activities and apathetic mood. By September, her speech had become m o r e hesitant and on occasion she would stop speaking in the middle o f a sentence. Left carotid and left vertebral angiography on September 10 showed hypovascularity of the mass. The previously demonstrated abnormal vascular pattern was not present (Fig. 3). A post-angiography CT scan delineated the left cerebral mass lesion (Fig. 4). B. Z a i a s , a n d W . J. M i c h e l s e n On September 12, 1985, the patient underwent a left temporal craniotomy with subtotal resection of the mass. Multiple fine vessels traversed the tumor, but no AVM was seen within the operative field. Histological examination disclosed foci of mild to moderate astrocytic proliferation, irregular dilated sinusoidal vascular channels, and an increased n u m b e r of small arterioles and veins. P a r e n c h y m a adjacent to blood vessels was sparsely cellular with abundant Rosenthal fibers and hemosiderin pigment. Other areas had astrocytic proliferation and pleomorphism (Fig. 5). Six months later (in March, 1986) the patient underwent a second subtotal resection when her condition acutely deteriorated following a probable seizure. A C T scan at that time evidenced further enlargement of the tumor. The histological diagnosis was increased cellularity, nuclear pleomorphism, and vascular proliferation consistent with anaplastic astrocytoma. Discussion FIG. 4. Computerized tomography scan obtained after left carotid and vertebral angiography showing a tumor of the left cerebrum. Review of Literature Coexistence of a vascular malformation and an intracerebral brain t u m o r is an infrequent occurrence. Review o f the literature discloses 13 previously reported cases (Table 1). In 1958, White, et al., 2~ in their review of intracranial vascular tumors found at necropsy, included a patient with a left temporal lobe cavernous h e m a n g i o m a and an astrocytoma of the septum pellucidum. Fine, et al., 4 in 1960 described a 15-year-old boy with a right parietal A V M and an intraventricular oligodendroglioma. They believed that the coexistence of the two lesions in the same patient was fortuitous. In 1966, Welcher and SeideP 9 described a patient with two discrete lesions in the same hemisphere: an AVM FIG. 5. Photomicrographs of the tumor. H & E, x 82. Left: Typical tumor field showing hypercellularity and pleomorphic nuclei. Right: Abnormal cluster of vessels within the tumor, possibly representing residua of prior vascular malformation. 800 J. Neurosurg. / Volume 7 2 / M a y , 1990 oa o..& e~ x. Cb, Seq 9, F 60, F 44, M 43, M 25, M 19, F 11, M 50, M 17, M 17, M ? 19, M t5, M 45, M Age (yrs), Sex 2 yrs ? 3 mos 30 mos (?) 2 yrs (?) 12 yrs several mos 5 yrs 5 mos 3 mos ?, 8 yrs ? 1.5 yrs 6 mos ? Duration - ? ? ? + - - - - + - ? + - - SAH Clinical Features carotids & vert angio, CT ? angio, CT angio, CT carotid & vert angio, CT CT with contrast rt carotid, angio, CT carotid angio, brain scan, CT It carotid angio rt carotid angio bilat carotid; angio ? carotid & vert anglo, vgram vgram, bilat carotid anglo ? Study + ? + + + + - + + + ? + + ? Mass Effect Radiography AVM & malignant astrocytoma AVM & oligodendroglioma in same mass residual tumor; no AVM astrocytoma "typical AVM" arteriovenous "angioma" AVM & hemangiobtastoma none oligodendroglioma astrocytoma-septum cav. hemangioma, It temporal Histopathology calcified vascular mass with pleomorphic neoplastic glia ? no AVM seen in operarive field angioma "tumor" rt frontal horn tumor rt parietal cortical AVM anaplastic astrocytoma glioblastoma angioma gliosarcoma Oligodendrogtioma AVM abn. tissue with calcium, oligodendroglioma in hemorrhage, cysts, & cortex, angioma; superfiabn. vessels cial cortex calcified, soft tissue with brown cyst; adherent to dura It frontal; discolored hemangioma & oligodentough & gelatinous tissue droglioma tumor with hemorrhagic cyst cyst & abn. vessels & tissue 2nd surg: postop scar rt frontal infilt, mass abn. meningeal vessels ? AVM of vermis superficial angioma abn. tissue, rt ventricle tumor of septum Gross Surgical Findings - - - - - - - - - + + + Autopsy Done AVM diagnosed by angio, initially; later disappeared; CT showed mass; same site AVM diagnosed radiographically tumor caused SAH, not AVM coexistent lesions subtotal resection, with no change in size of residual mass after 5 yrs tumor appeared 5 yrs later in same site as hemangioma secondary neoplastic glial changes in response to vascular malformation SAH & mass effect may be AVM & t u m o r Cb lg abn. vessels & unusual tumor vascularity; may suggest AVM & tumor fibrillary astrocytoma discovered at autopsy, same hemisphere, different sites first report of intermixture of lesions "fortuitous association" cav. hemangiomas liver & lung; ? genetic syndrome Remarks * M = malformation; T = tumor; Sep = separate; Cb = combined; Si = simultaneous; Seq = sequential; SAH = subarachnoid hemorrhage; vgram = ventriculogram; angio = angiogram; abn. = abnormal; car = cavernous; CT = computerized tomography; vert = vertebral artery; AVM = arteriovenous malformation. ~ Same site, different time. t990 et aL, M & T = It parietotemporal Sep, Si M = It occipital T = It temporal Goodkin, Cb, Seq~" M = rt rolandic T = rt parietal Licata, et aL, 1986 Sep, Si M = rt parietal T = rt frontal horn Cb, Si M & T = rt ternporo-occipital Fischer, et al., 1982 MartinezLage, et aL, 1986 Cb, Seqt M & T = It frontal Zuccarello, et aL, 1979 Cb, Si Cb, ? M & T = It temporal Crowdl, et aL, 1975 M & T = rt frontal Cb, Si M & T = rt temporal Chee, et aL, 1985 Sep, Si Sep, Si Weleher & M & T = ? Seidel, 1966 M = rt frontal meninges, T = rt frontal Cb, Si M &T = ? Raynor & Kingman, 1965 Heffner, aL, 1971 Sep, Si M = rt parietal, T = intravent, Fine, et aL, 1960 Sep, Si ante of Lesions M = It temporal, T = septum Location Appear- White, et ak, 1958 Authors & Year TABLE 1 Summary of 14 reported cases of coexisting vascular malformation and intracerebral brain tumor* t~ r co t~ O t~ > < R. Goodkin, B. Zaias, and W. J. Michelsen and an astrocytoma. The brain tumor, discovered at necropsy, had not been suspected during life. They considered their report o f coexisting lesions to be the first, apparently unaware o f the reports of Fine, et al., or White, et al. In 1965, R a y n o r and Kingman ~4 reported a patient with a hemangioblastoma and a vascular malformation occurring as one lesion. These authors credit themselves with presenting the first case of two intermixed lesions within the same mass, as welt as the demonstration of an increase in size and vascularity of the lesion. In 1971, Heffner, et al.,8 reported a patient whose initial radiographic study suggested "vascular glioma;" however, surgery' disclosed a nonvascular astrocytoma and a "typical A V M . " Crowell, et at., 2 described a patient who presented with subarachnoid hemorrhage (SAH) and whose angiogram showed an avascular mass; an oligodendroglioma and AVM were disclosed at the same site. Zuccarello, et al., "-~ reported the case o f a patient with an intermixed AVM and malignant astrocytoma. They suggested that the association of a t u m o r and vascular malformation represented a definite entity and not a coexistence of individual lesions. In 1982, Fischer, et al., 5 described two patients with glial neoplasms and cavernous hemangiomas. In one o f these, the lesions were combined and coexistent; in the other, an oligodendroglioma apparently subsequently grew at the same site as the hemangioma. Chee, et al., ~ reported a case of coexisting oligodendroglioma and angioma in which the CT scan had not shown the angioma. An interesting case is that o f Martinez-Lage, et a L , ~2 in which the SAH is believed to have originated from the intraventricular oligodendroglioma rather than the parietal AVM. Licata, et al., ~ reported two patients with central nervous system (CNS) parenchymal tumors and AVM's; one had coexistent lesions while the other patient's tumor appeared subsequently at the site o f the former angioma. O f these 14 cases, including ours, the vast majority (11 patients) had simultaneous occurrence or coexistence of the two lesions, whereas three apparently showed subsequent development o f a t u m o r at the same site as the previously diagnosed vascular malformation (Table 2). A m o n g the 11 simultaneously occurring lesions, six were coexistent but separate within the same hemisphere,8.1H2,~9 ipsilateral ventricle, 5 or septum pellucidum 2~ and five were coexistent but combined or intermixed. ~4 In the remaining three patients, tumors were found at varying periods o f time after the initially diagnosed vascular lesion: 5 years, 5 30 months, ~ and 22 months (our case). A separate group of combined or coexistent neural tumors and vascular malformations is that of peripheral nervous system neurilemomas and angiomas reviewed in 1979 by Kasantikul and Netskyfl They described eight cases o f their own in addition to five culled from the literature and proposed that a c o m m o n embryological origin from ectomesenchyme could explain their simultaneous occurrence. We have not included this group in our tabulation, since we are concerned with 802 TABLE 2 S u m m a r y o f sequence and location o f lesions Authors & Year coexistent: separate lesions (ipsilateral) White, et aL, 1958 Fine, et al,, 1960 Welcher & Seidet, 1966 Heffner, et al., 1971 Martinez-Lage, et al., 1986 Licata, et al., 1986 total cases coexistent: combined within one lesion (site) Raynor & Kingman, 1965 Crowell, et aL, 1975 Zuccarello, et al., 1979 Fischer, et al., 1982 Chee, et aL, 1985 total cases "subsequent:" one lesion after the other (same site) Fischer, et al., 1982 Licata, et al., 1986 Goodkin, et al., 1990 total cases * Tumor in septum. No. of Cases 1" 1 1 1 1 1 6 1 1 1 1 1 5 1 1 1 3 intracranial CNS parenchymal tumors and associated vascular lesions. Other features include an age range at occurrence from 11 to 25 years in patients with oligodendrogliomas and vascular malformations, with the only exception being a 43-year-old man. In cases in which the patient's sex was known, the majority were male: all five cases of oligodendroglioma and four of five cases of astrocytoma. Etiology and Diagnosis The question raised by the present case report is that of the possible occurrence of two different CNS lesions, either simultaneously or sequentially within the same patient, or the existence throughout the clinical course o f only one lesion. Difficulties encountered in pathological and radiological interpretations can thwart a clear resolution of the issue. The gross and histological features of brain tumors (gliomas) and vascular malformations have m a n y similarities. In 1937, Trnnis ~s first described arteriovenous shunting and abnormal blood vessels observed at surgery for a glioblastoma multiforme. Since then, other vascular changes within malignant gliomas have been well described ~3 and include: increased small blood vessels, mainly capillaries, excessively convoluted masses of capillaries ("glomeruloids'); sinusoidal channels; and prominent endothelial and adventitial proliferation affecting all sizes of vessels. Tortuous ectatic vessels, aneurysmal dilations, and arteriovenous anastomoses with early draining veins as well as thrombosed vessels in varying stages of organization and recanalization may be seen in both tumors J. Neurosurg. / V o l u m e 72/May, 1990 A V M and glioma at same cerebral site TABLE 3 Radiographic diagnoses in 12 cases* Ventriculographic Findings Angiographic Findings CT Scan Findings -- intraventricular mass rt A V M ; h y d r o c e p h a l u s ; no m a s s seen -- angio, m i s s e d t u m o r , ventriculogram missed AVM -- -- p o s t e r i o r fossa midline mass c a r o t i d & vertebral a r t studies, initially n o r m a l -- studies d i d n o t d i a g nose vascular malformation Heft'ner, et e r o d e d sella d e p r e s s e d rt orbital p l a t e low rt frontal abnormality -- c a r o t i d arts i n d i c a t e d rt frontal m a s s w i t h a b n o r m a l vessels & e a r l y v e n o u s filling -- initial a n g i o , d i a g nosed "vascular" glioma; abnormal tumor vascular pattern suggested A V M + tumor Crowell, et al., 1975 normal rt t e m p o r a l abnormality rt t e m p o r a l lobe cyst in c o m m u n i c a t i o n with ventricle rt c a r o t i d art i n d i c a t e d large, a v a s c u l a r , i n t r a temporal mass -- n o s u g g e s t i o n o f vascular malformation Zuccarello, et al., 1979 normal It t e m p o r a l abnormal uptake -- It c a r o t i d a r t i n d i c a t e d temporal mass with tort u o u s vessels & a r t e r i o v e n o u s fistula -- angio, d i d d i a g n o s e vascular malformation, but not tumor Fischer, et al., 1982 It frontal C a ++ It frontal abnormality -- -- carotid art study normal -- rt c a r o t i d a r t i n d i c a t e d s t r e t c h e d vessels; n o p a t h o l o g i c vessels o r t u mor blush It f r o n t a l Ca++; n o m a s s effect o r e n h a n c e m e n t rt t e m p o - o c c i p i t a l w i t h Ca++; h y d r o c e p h a l u s ; n o abnormal enhancement n o s u g g e s t i o n o f vascular malformation n o s u g g e s t i o n o f vascular malformation -- -- -- rt f r o n t a l m a s s with Ca++; m a s s effect; slight enhancement n o s u g g e s t i o n o f vascular malformation on CT rt c a r o t i d a r t study; rt parietal A V M ; h y d r o cephalus; n o a b n o r m a l v a s c u l a r stain at site; It c a r o t i d & vertebral a r t s normal rt lateral v e n t r i c u l a r byperdense mass with faint enhancement angio, m i s s e d m a s s ; CT missed vascular malformation angio. & C T initially correct; a n g i o , c o r rect, C T i n c o r r e c t 2rid t i m e Authors & Year X-Ray Findings Brain Scan Findings Fine, et al., 1960 -- Raynor & Kingman, l 965 al., 1971 rt t e m p o r o occipital C a ++ mass Chee, et al., 1985 -- MartinezLage, et al., 1986 n o C a ++ no intracranial hypertension Licata, et al., 1986 -- -- -- rt c a r o t i d study: rt rolandic A V M 2~ yrs later: rt parietal m a s s with a b n o r m a l v a s c u l a r ity: t u m o r ? ? ? It occipital a n g i o m a no contrast: normal; with c o n t r a s t : p a r i e t a l angio m a ; 2 ~ yrs: rt parietal m a s s w i t h p e r i p h e r a l enh a n c e m e n t ; diagnosis: abscess It t e m p o r a l g l i o m a bilat c a r o t i d & It vertebral a r t study: It c e n t r o sylvian A V M 2 yrs later: h y p o v a s c u l a r mass without abnormal vascularity m a r k e d l y e n h a n c i n g It c e n t r o s y l v i a n m a s s with d r a i n i n g veins i n d i c a t i n g vein o f G a l e n i n c r e a s i n g size o f It cerebral mass G o o d k i n , et al., 1990 Remarks angio, m i s s e d m a s s ; CT missed vascular malformation initial studies d i a g n o s e d A V M ; subseq u e n t studies: d i s a p pearance of AVM, i n c r e a s i n g size o f h y p o v a s c u l a r m a s s in s a m e site * A V M = a r t e r i o v e n o u s m a l f o r m a t i o n ; C T = c o m p u t e r i z e d t o m o g r a p h y ; angio. = a n g i o g r a m ; - - = n o t d o n e . V a s c u l a r m a l f o r m a t i o n n o t initially d i a g n o s e d : a) b y a n g i o in five o f 11 cases with a n g i o g r a p h y done; b) b y C T in five o f s e v e n cases w i t h C T d o n e . J. N e u r o s u r g . / V o l u m e 72 / M a y , 1 9 9 0 803 R . G o o d k i n , B, Z a i a s , a n d W . J. M i c h e l s e n and vascular malformations. The AVM, particularly, can exhibit any or all of these features, in addition to abnormally structured arteries and veins. Radiographic vascular changes of tumors can overlap with those of vascular malformations, causing diagnostic confusion. The presence o f abnormal afferent and efferent blood vessels and arteriovenous shunting of blood, in the absence o f mass effect and edema, usually leads to the radiographic diagnosis o f an AVM. Difficulty may arise in differentiating an AVM which was ruptured with h e m a t o m a formation from a t u m o r with mass effect. Kumar, et aL, ~~ reviewed 60 cases o f clinically ruptured AVM's, in which high-resolution CT demonstrated local or remote mass effect in 33 patients. There are similarities between the C T scan appearance o f their cases, as illustrated in their Figs. 1 and 3, and the CT scan findings in our case. Vascular malformations may simulate tumors, showing high density on noncontrast CT but not appearing on angiography (socalled "cryptic" angiomas, now more readily appreciated by a characteristic magnetic resonance (MR) image appearance). By contrast, a recent report by Rigamonti, et al., ~ describes a patient with a right frontal venous malformation diagnosed by angiography, CT, and MR imaging who 1 year later developed a glioblastoma in the same site. They suggested that the initial studies did not exclude the possibility that the venous malformation represented a rather p r o m i n e n t venous drainage of the subsequently diagnosed gliobtastoma. Multiple etiologies for the association of vascular malformations and tumors within the same patient have been proposed. These include: fortuitous association; 4'~-~genetic predisposition; 2~ a distinct entity, possibly of viral origin, with biological potential to evolve along different lines; 5 a secondary or reactive neoplastic glial change to a previously existing vascular malformation; 2j and the influence o f a t u m o r angiogenesis factor. 6,7,~7 Another theory was that of Russell and Rubinstein,~6 who rejected the concept of two different lesions, diagnosing instead either "hypervascularized t u m o r or undue glial reaction." Since concomitant histopathological sampling and radiographic studies throughout the duration o f these lesions have not been performed in any of these cases, these proposals remain speculative. O f the cases reviewed, a vascular malformation was not initially diagnosed by angiography in five of 11 cases 3'5'8"j4 or with CT ~,5,~'~2 (Table 3). In a case cited by Heffner, et al., 8 the angiographic pattern of abnormal vasculature associated with a frontal mass was considered to be a "vascular glioma." In the two cases of Fischer, et al., 5 the initial angiograms were normal in one and showed mass effect but no "pathologic vessels, early draining veins, or t u m o r blush" in the other. In the six cases in which the vascular malformation was diagnosed by angiography, a separate mass lesion was suspected in only two: by ventriculogram in one 4 and by CT in the other. 12 In the present case, the angiographically abnormal 804 vessels, initially felt to represent an AVM, regressed and disappeared over a period of 22 months. Within the same period a progressively enlarging hypovascular mass developed at the same site. Two biopsies with subtotal resection, obtained 6 months apart, confirmed a diagnosis of anaplastic astrocytoma without evidence of a vascular malformation. It is the our contention that this case represents an AVM in which a malignant (anaplastic) astrocytoma grew, replacing the AVM. We realize that this case may just as well represent a single lesion (anaplastic astrocytoma) in which the vascular pattern initially simulated the angiographic appearance of an AVM. It is suggested that future research may include, a m o n g other goals, the search for a t u m o r angiogenetic factor in resected vascular malformations in the hope of defining a possible relationship between the two lesions. Acknowledgment The authors wish to thank Dr. Charles B. Wilson for his review of this case and recommendations regarding management of the patient. References 1. Chee CP, Johnson R, Doyle D, et at: Oligodendroglioma and cerebral cavernous angioma. Case report. J Neurosnrg 62:145-147, 1985 2. Crowell RM, DeGirolami U, Sweet WH: Arteriovenous malformation and oligodendroglioma. Case report. J Neurosurg 43:108-11 l, 1975 3. Dykstra PC: The pathology of acoustic neuromas. Arch Otolaryngol 80:605-616, 1964 4. Fine RD, Paterson A, Gaylor JB: Recurrent attacks of subarachnoid haemorrhage in the presence of a cerebral angioma and intraventricular oligodendroglioma. Scot Med J 5:342-346, 1960 5. Fischer EG, Sotrel A, Welch K: Cerebral hemangioma with glial neoplasia (angioglioma?). Report of two cases. J Neurosurg 56:430-434, 1982 6. Folkman J: Tumor angiogenesis. Adv Cancer Res 19: 331-358, 1958 7. Folkman J, Merler E, Abernathy C, et al: Isolation of a tumor factor responsible for angiogenesis. J Exp Med 133:275-288, 1971 8. Heffner RR Jr, Porro RS, Deck MDF: Benign astrocytoma associated with arteriovenous malformation. Case report. J Neurosurg 35:229-233, 1971 9. Kasantikul V, Netsky MG: Combined neurilemmoma and angioma. Tumor of ectomesenchyme and a source of bleeding. J Neurosnrg 50:81-87, 1979 10. Kumar AJ, Vifiuela F, Fox AJ, et al: Unruptured intracranial arteriovenous malformations do cause mass effect. AJNR 6:29-32, 1985 11. Licata C, Pasqualin A, Freschini A, et al: Management of associated primary cerebral neoplasms and vascular malformations. 2: lntracranial arterio-venous malformations. Acta Neurochir 83:38-46, 1986 12. Martinez-Lage JF, Poza M, Esteban JA, et al: Subarachnoid hemorrhage in the presence of a cerebral arteriovenous malformations and an intraventricular oligodendroglioma: case report. Neurosurgery 19:125-128, 1986 13. Nystrrm S: Pathological changes in blood vessels of human glioblastoma muttiforme: comparative studies using plastic casting, angiography, light microscopy, and elecJ. Neurosurg. / V o l u m e 72 /]t4ay, 1990 A V M and glioma at same cerebral site tron microscopy, and with reference to some other brain tumours. Acta Pathoi Microbiol Scand 49 (Sappl 137): 1-83, 1960 14. Raynor RB, Kingman AF Jr: Hemangioblastoma and vascular malformations as one lesion. Arch Neurol 12: 38-48, 1965 15. Rigamonti D, Spetzler RF, Drayer BP, et al: Appearance of venous malformations on magnetic resonance imaging. J Neurosurg 69:535-539, 1988 16. Russell DS, Rubenstein L J: Pathology of Tumors of the Nervous System, ed 2. Baltimore: Williams & Wilkins, 1963, p 122 17. Suddith RL, Kelly PJ, Hutchison HT, et al: In vitro demonstration of an endothelial proliferation factor produced by neural cell lines. Science 190:682-684, 1975 18. T6nnis W: Die bedeutung der "Angiographie cerebrale" fur dieindikationsstellung zur operation von hirngeschwulsten. Lisboa Med 14:773-780, 1937 J. Neurosurg. / Volume 7 2 / M a y . 1990 19. Welcher ER, Seidel K: Kombination eines Angioma arteriovenosum aneurysmaticum mit einem Astrocytom. Dtsch Z Nervenheilk 189:231-239, 1966 20. White R J, Kernohan JW, Wood MW: A study of 50 intracranial vascular tumors found incidentally at necropsy. J Neuropathol Exp Neurol 17:392-398, 1958 21. Zuccarello M, Giordano R, Scanarini M, et al: Malignant astrocytoma associated with arteriovenous malformation. Case report. Acta Neuroehir 50:305-309, 1979 Manuscript received June 19, 1989. Accepted in final form October 4, 1989. Address reprint requests to: Robert Goodkin, M.D., Department of Neurological Surgery, Harborview Medical Center, ZA-86, 325 Ninth Avenue, Seattle, Washington 98104. 805