J Neurosurg 72:692-697, 1990
Management of dural arteriovenous malformations of the anterior cranial fossa NElL A. MARTIN, M.D., WESLEY A. KING, M.D., CHARLES B. WILSON, M.D., STEPHEN NUTIK, M.D., L. PHILLIP CARTER, M.D., AND ROBERT F. SPETZLER, M.D.
Department of Surgery, Division of Neurosurgery, School of Medicine, University of Calijornia, Los Angeles, California; Department of Neurological Surgery, School of Medicine, University of California, San Francisco, California; Department of Neurosurgery, Kaiser Permanente Medical Center, Redwood City, California; and Division of Neurological Surger3,; Bartvw Neurological Institute, Phoenix, Arizona ~," Eight patients with dural arteriovenous malformations (AVM's) of the anterior cranial fossa are presented, and the pertinent literature is reviewed. Unlike cases of dural AVM's in other locations, sudden massive intracerebral hemorrhage was the most frequent reason for presentation. Other symptoms included tinnitus, retro-orbital headache, and a generalized seizure. The malformations were supplied consistently by the anterior ethmoidal artery, usually in combination with other less prominent feeding vessels. The lesion's venous drainage was through the superior sagittal sinus via a cortical vein; in addition, in two cases a subfrontal vein drained the AVM. A venous aneurysm was encountered near the site of anastomosis with the dural feeder in most cases, and was found in all patients who presented with hemorrhage. The AVM was obliterated surgically in six patients, with favorable results achieved in five. One patient died postoperatively from a pulmonary complication. Because of their anatomy and proclivity for hemorrhage, these vascular malformations represent a unique group of dural AVM's. Surgical management of anterior fossa dural AVM's carries low morbidity, and is indicated when the lesions have caused hemorrhage or when there is an associated venous aneurysm. KEY WORDS anterior ethmoidal artery 9 anterior fossa arteriovenous malformation 9 cerebral hemorrhage
URALarteriovenous malformations (AVM's) are rare vascular anomalies that most frequently involve the cavernous, transverse, or sigmoid sinuses. 1"2"8"12"14"18"19"'-5 Most intracranial dural AVM's present with relatively benign symptoms such as headache or subjective bruit, with only a small percentage of these lesions causing intracranial hemorrhage. Some remain asymptomatic. Those in the anterior cranial fossa, however, form a distinct subgroup that has an unusually high incidence o f intracerebral hemorrhage. Anterior fossa dural A V M ' s were first reported in 1963, j5 and have been reported only sporadically since that time. 3"5-8'~ ~,~9,22.2325In this report, we review eight new cases, with a focus on the unique anatomic features that have relevance to their clinical presentation, natural history, and surgical management. Summary of Cases
The features o f eight patients with dural AVM's of the anterior cranial fossa were collected from a retrospective review of clinical, radiological, and surgical 692
9 dural lesion
records (Table 1). There were seven men and one woman, ranging in age from 44 to 61 years, with a mean age of 52 years.
Presenting Symptoms The presenting symptom in four patients was apoplectic. In these cases, computerized tomography (CT) showed evidence of an acute frontal hemorrhage with mass effect (Fig. 1). All of these patients were comatose. One patient presented with a small spontaneous occipital hemorrhage; cerebral angiography performed to evaluate the cause of the hemorrhage failed to show a vascular lesion in the occipital region, but demonstrated an incidental small dural A V M of the anterior fossa. One patient presented with a generalized seizure, and was found on CT to have a small frontal hemorrhage without mass effect. No preceding neurological symptom was elicited from any o f the patients who sustained hemorrhages, and there was no history o f trauma. Two patients had no evidence of intracranial hemorrhage. One of these patients presented with tinnitus, and dur-
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AVM's of the anterior cranial fossa TABLE 1 Clinical summary of eight patients with anterior fossa dural A V~I's* Case No. 1 2
Age (yrs), Sex 61, M 54, M
Clinical Presentation ICH, obtundation ICH, obtundation
48, M 50, M
ICH, seizure incidental (occipital hemorrhage) tinnitus
AEA (bilat) AEA (bilat), STA
superficial, SSS superficial, SSS subfrontat superficial, SSS superficial, SSS
AEA, ACA, STA AEA
Aneurysmal Dilatation yes yes
yes, AD excised yes
yes, falx excised no
Surgical Outcome died good good
AEA, STA, IMA superficial, SSS yes no (bilat) subfrontal, BV 6 54, M retro-orbital headAEA, STA, IMA superficial, SSS no yes good ache (bilat) 7 44, M ICH, obtundation AEA superficial, SSS yes yes good 8 50, F ICH, obtundation AEA, MMA superficial, SSS yes yes, AD excised good * Abbreviations: AVM = arteriovenous malformation; ICH = intracerebral hemorrhage; AEA = anterior ethmoidal artery; ACA = anterior cerebral artery; STA = superficial temporal artery; IMA = internal maxillary artery; MMA = middle meningeal artery; SSS = superior sagittal sinus; BV = basal vein; AD = aneurysmal dilatation.
FIG. 1. Case 8. Left: Computerized tomography scan showing a large intraparenchymal hemorrhage in the left frontal lobe with mass effect and intraventricular extension. Right: Left common carotid angiogram. The venous aneurysm which was the source of hemorrhage is demonstrated (upper arrow), The two smaller arrows indicate the ophthalmic and anterior ethmoidal arteries. The nidus in the dura is located in the region of the open arrow.
ing the course o f t h e e v a l u a t i o n was f o u n d to have a n u n r u p t u r e d d u r a l A V M o f t h e a n t e r i o r fossa. T h e seco n d p a t i e n t p r e s e n t e d with severe persistent retro-orbital h e a d a c h e , w h i c h led to i d e n t i f i c a t i o n o f t h e d u r a l AVM by CT and angiography. Radiographic Features C o m p u t e r i z e d t o m o g r a p h y was p e r f o r m e d in all cases, T h e C T scan s h o w e d a n a c u t e i n t r a c e r e b r a l h e m o r r h a g e w i t h i n t h e frontal l o b e in five patients, T h e h e m a t o m a i n v o l v e d t h e a n t e r o m e d i a l aspect o f the J. Neurosurg, / Volume 72~May, 1990
frontal p o l e a n d , in several cases, e x t e n d e d v e n t r a l l y to the a r e a o v e r l y i n g the c r i b r i f o r m plate. M a s s effect was e v i d e n t e x c e p t i n Case 3 w h e r e the h e m a t o m a was small. A r e m o t e a n d u n r e l a t e d occipital h e m o r r h a g e was seen in o n e p a t i e n t . Significant s u b a r a c h n o i d h e m orrhage was n o t o b s e r v e d in a n y o f t h e cases. I n t h e t w o patients w i t h o u t h e m o r r h a g e , a s e r p e n t i n e p a t t e r n o f e n h a n c e m e n t , suggestive o f v a s c u l a r structures, was seen in the a n t e r o m e d i a l f r o n t a l lobe. Internal a n d e x t e r n a l c a r o t i d a n g i o g r a p h y was p e r f o r m e d in all cases. In all eight patients, t h e p r i m a r y source o f arterial s u p p l y was from the ipsilateral a n t e r i o r e t h m o i d a l artery, w h i c h is a t e r m i n a l b r a n c h o f t h e o p h t h a l m i c a r t e r y (Fig. 2). C o n t r a l a t e r a l i n t e r n a l carotid artery i n j e c t i o n s s h o w e d filling o f the m a l f o r m a tion, a p p a r e n t l y t h r o u g h i n t e r e t h m o i d a l arterial a n a s tomoses. In o n e p a t i e n t (Case 3), in w h o m a p o r t i o n o f the m a l f o r m a t i o n a p p e a r e d to involve the a n t e r i o r falx, a tiny frontal b r a n c h o f the a n t e r i o r cerebral a r t e r y p a r t i c i p a t e d in t h e m a l f o r m a t i o n . External c a r o t i d artery supply was seen in five cases (Fig. 3). T h e i n t e r n a l m a x i l l a r y a r t e r y p a r t i c i p a t e d b y a n a s t o m o s e s with distal b r a n c h e s o f the o p h t h a l m i c artery in two cases, a n d t h e m i d d l e m e n i n g e a l a r t e r y p a r t i c i p a t e d in o n e case. I n f o u r cases a b r a n c h o f t h e superficial t e m p o r a l a r t e r y p e n e t r a t e d t h e c a l v a r i a a n d s u p p l i e d b l o o d flow to t h e malformation through dural anastomoses. V e n o u s d r a i n a g e was p r i m a r i l y i n t o the pial veins, w h i c h d r a i n e d m e d i a l l y i n t o t h e s u p e r i o r sagittal sinus. A d d i t i o n a l l y , in t w o cases s u b f r o n t a l pial veins d r a i n e d posteriorly t o w a r d t h e r e g i o n o f t h e s p h e n o p a r i e t a l a n d c a v e r n o u s sinuses. I n p a t i e n t s with h e m o r r h a g e f r o m the d u r a l A V M , c e r e b r a l a n g i o g r a p h y c o n s i s t e n t l y demonstrated an aneurysmal dilatation of the venous c h a n n e l s ( v e n o u s a n e u r y s m ) n e a r the site o f t h e d u r a l to-pial a n a s t o m o s i s (Fig. 1). T w o o f t h e p a t i e n t s w i t h u n r u p t u r e d A V M ' s h a d d i r e c t c o n n e c t i o n s to t h e sag693
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FIG. 2. Drawing of a typical anterior fossa dural arteriovenous malformation indicating the anterior ethmoidal artery, nidus, and venous aneurysm.
ittal sinus with minimal involvement of pial veins, and with no aneurysmal dilatation (Fig. 4).
Operative Procedure Surgical treatment was carried out in the five patients with hemorrhage and in the one patient with retroorbital headache. The vascular malformation was approached via a low-frontal craniotomy in each case and, upon exposure of the cortical surface, arterialized cortical veins were identified. In one case, the venous aneurysm ruptured during evacuation of the frontal lobe h e m a t o m a resulting in moderately brisk arterial bleeding, which was controlled by clipping the fragile sac. After partial evacuation of the frontal hematoma, retraction of the frontal lobe revealed the vascular connection between the dura in the region of the cribriform plate and the pial vessels on the anterior inferior aspect of the frontal lobe (Fig. 5). Once the vascular connection between the dura and frontal lobe was coagulated and divided, the aneurysm and the arterialized pial veins collapsed. In no case was extensive excision of the dura of the anterior fossa floor required. However, the falx was excised in one case when its anterior portion was involved by the AVM. Entry into the orbit was not required in any case, nor was occlusion of the ophthalmic artery. Operative Results All of the patients recovered neurologically after surgery except for Case 1. This patient, who was co694
matose preoperatively, did not recover consciousness after surgery and ultimately died from a pulmonary embolism. Postoperative angiography confirmed complete obliteration of the AVM, even in the patients in w h o m the arterialized pial venous system was not excised (Fig. 6).
Discussion Dural A V M ' s comprise 10% to 15% of all intracra-
n i a l A V M ' s . L8"17 The great majority of these lesions
involve the dural wall of the cavernous sinus or the transverse and sigmoid sinuses. Dural A V M ' s of the anterior fossa are particularly unusual; only approximately 20 cases have been reported, and they make up less than 10% of the cases in the large reviews? Dural A V M ' s are typically fed by meningeal arteries and drain into adjacent dural sinuses. Occasionally, pial veins are recruited when venous hypertension or occlusion of the sinus gives rise to retrograde flow into the cerebral veins, which ordinarily empty into the involved s i n u s . 9'2~ Dural A V M ' s of the anterior cranial fossa almost universally involve the dura in the region of the cribriform plate and the anterior falx. The principal arterial supply comes from the ipsilateral anterior ethmoidal artery. These malformations m a y recruit additional supply through anastomoses with the contralateral anterior ethmoidal artery, distal branches of the internal maxillary artery, or middle meningeal branches or from
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AVM's of the anterior cranial fossa
FIG. 3. Left common carotid angiograms, early arterial phase, in Case 5. Left: This shows a branch of the ophthalmic artery (small arrows) feeding the dural arteriovenous malformation (AVM) nidus (large arrow). An aneurysm clip was previously used to treat a contralateral middle cerebral artery aneurysm. Right: Distal branches of the internal maxillary artery (lower arrows) have been recruited by the AVM. The supraorbital branch (arrowheads) and a transosseous branch (upper arrows) of the superficial temporal artery also supply the AVM. In this case drainage is through a subfrontal pial vein.
superficial t e m p o r a l artery branches t h r o u g h transcalvarial anastomoses. Dural A V M ' s o f the anterior cranial fossa have a distinct pattern o f venous drainage. Drainage is primarily into pial veins o f the anterior frontal lobe from which they e m p t y into the superior sagittal sinus or posteriorly t o w a r d the cavernous sinus.l~ The configuration o f these lesions in this way is reminiscent o f dural A V M ' s o f the spine. 2~ In 85% o f reported cases, the venous side o f these m a l f o r m a t i o n s has involved a large venous a n e u r y s m (or varix). This varix appears to be the source o f the h e m o r r h a g e which is a c o m m o n complication o f anterior fossa dural A V M ' s . Eighty percent o f previously reported cases and five (63%) o f our cases presented with hemorrhage. ~~ The hemorrhage was always into the frontal lobe a n d a venous a n e u r y s m was present in each case. W h e n an a n e u r y s m was not present, the lesion caused n o n h e m o r r h a g i c s y m p t o m s or was an incidental finding. H e m o r r h a g e m a y be massive a n d life-threatening, as it was in four o f our patients. Dural A V M ' s in other locations present with h e m o r r h a g e less frequently, typically from pial veins which have been recruited for drainage. 4.j3~6 Approximately 15% o f the patients with dural A V M ' s reviewed by H o u s e r and associates 8 had intracranial hemorrhage (usually s u b a r a c h n o i d hemorrhage from ruptured pial vessels). In o u r series a n d in previously reported cases o f anterior fossa dural A V M ' s , there has been a striking p r e d o m i n a n c e o f males. This contrasts with the female p r e d o m i n a n c e f o u n d in dural A V M ' s o f the cavernous sinus. The male:female ratio f o u n d a m o n g anterior
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FIG. 4. Case 4. Right common carotid angiogram showing an incidentally found anterior fossa arteriovenous malformation. The malformation drains directly into the superior sagittal sinus (large arrows). The nidus is clearly seen distal to the ophthalmic and ethmoidal arteries (small arrows). fossa dural A V M ' s is strikingly similar to that for dural A V M ' s o f the spine. 2~ T h e r e was no history o f basal skull fracture or significant t r a u m a in our cases, a n d this has been rare in o t h e r reports. N o other predisposing causes have been identified. It is our belief t h a t
FIG. 5. Surgical drawing with the left frontal lobe elevated to reveal the arterialized vascular connection between the dura in the region of the cribriform plate and the pial venous system.
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FIG. 6. Internal carotid angiograms in Case 2. Left: Preoperative appearance of the lesion. Solid arrows identify the draining veins. The open arrow shows drainage into the posterosuperior compartment of the cavernous sinus. Right: Postoperative result after dividing the vascular connection between the anterior fossa dura and the frontal lobe. There is no filling of either the nidus (arrow) or the draining veins.
these malformations are congenital, and that symptoms occur only after long-standing h e m o d y n a m i c stress has caused dilatation then rupture o f a draining venous channel. Surgical treatment is straightforward. The key step is occlusion of the vascular connection between the dura o f the cribriform plate area a n d the pial vessels. With a low frontal craniotomy, this requires minimal frontal lobe retraction. Evacuation o f an intracerebral hemat o m a m a y be necessary to allow safe retraction of the frontal pole, but care should be taken to avoid rebleeding from the arterialized veins. I f the anterior aspect of the falx is involved, this should be excised. Although we excised the venous a n e u r y s m in two cases, this is probably not necessary. With occlusion of the duralpial connection, the venous side o f the malformation will collapse and thrombose. Again, in this respect, a parallel can be drawn between anterior fossa dural A V M ' s and dural A V M ' s of the spine. Surgery is the t r e a t m e n t o f choice. Only one patient in our series did not recover after surgery. This patient died from complications related to his failure to recover from the effects of the initial hemorrhage. Previously reported series have shown a very high success rate for complete A V M obliteration, with minimal morbidity. Embolization or other forms o f endovascular therapy, given the present state o f technical development, appear to be impractical because o f the difficulty of catheterizing the o p h t h a l m i c artery, and seem to carry an 696
unacceptable risk of visual c o m p r o m i s e due to occlusion of retinal branches. Conclusions Drawing upon our experience and that described in the previously reported cases, the following recommendations are made: 1. Dural A V M ' s of the anterior fossa should be included in the differential diagnosis of spontaneous intracerebral hemorrhage involving the anteromedial frontal lobe (particularly in middle-aged males). 2. Surgical treatment should consist of division of the vascular connection between the dura and the pial vessels, a procedure that carries low risk. 3. Surgery is clearly indicated in cases where there has been intracerebral hemorrhage related to the dural AVM. 4. Surgery is indicated in unruptured cases when a venous aneurysm is demonstrated, because of the apparently high risk of hemorrhage. Acknowledgments The authors thank Richard H. Schwartz, M.D., and Richard M. Hodosh, M.D., who each contributed a case to this series, and Steven Harrison for the illustrations. References 1. Aminoff M J: Vascular anomalies in the intracranial dural J. Neurosurg. / Volume 72 / May, 1990
AVM's of the anterior cranial fossa mater. Brain 96:601-612, 1973 2. Aminoff M J, Kendall BE: Asymptomatic dural vascular anomalies. Br J Radiol 46:662-667, 1973 3. Bitoh S, Nakagawa H, Arita N, et al: Dural arteriovenous malformation in the anterior fossa. Case report. Neurol Med Chir 21:131-134, 1981 4. Castaigne P, Bories J, Brunet P, et al: Les fistules art6rioveineuses m6ning6es pures ~ drainage veineux cortical. Rev Neurol 132:169-181, 1976 5. Dardenne G J: Dural arteriovenous anomaly fed by et~moidal arteries. Surg Neurol 10:384-388, 1978 6. Enomoto H, Goto H, Murase M: Subarachnoid hemorrhage due to a cerebral aneurysm at the anastomotic site between the frontoorbital artery and the anterior ethmoidal artery: a case report. Neurosurgery 17:335-337, 1985 7. Handa J, Shimizu Y: Dural arteriovenous anomaly supplied by the anterior falcine artery. Neuroradiology 6: 212-214, 1973 8. Houser OW, Baker HL Jr, Rhoton AL Jr, et al: Intracranial dural arteriovenous malformations. Radiology 105: 55-64, 1972 9. Houser OW, Cambell JK, Campbell R J, et al: Arteriovenous malformation affecting the transverse dural sinus - an acquired lesion. Mayo Clin Proe 54:651-661, 1979 10. Ito J, Imamura H, Kobayashi K, et al: Dural arteriovenous malformations of the anterior cranial fossa. Neuroradiology 24:149-154, 1983 11. Katayama Y, Tsubokawa T, Moriyasu N, et al: Dural arteriovenous malformations in the anterior cranial fossa. No Shinkei Geka 8:1079-1085, 1980 12. Kosnik EJ, Hunt WE, Miller CA: Dural arteriovenous malformations. J Neurosurg 40:322-329, 1974 13. Lasjaunias P, Chiu M, Ter Brugge K, et al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:724-730, 1986 14. Lasjaunias P, Manelfe C, Chiu M: Angiographic architecture of intracranial vascular malformations and fistulas - - pretherapeutic aspects. Neurosurg Rev 9:253-263, 1986
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15. Lepoire J, Montaut J, Bouchot M, et al: Anevrismes art6rior-veineux intrafrontaux vascularis6s par l'art6re ethmoidale ant&ieure. A p r o p o s de trois observations. Neurochirurgie 9:159-166, 1963 16. Malik GM, Pearce JE, Ausman JI, et al: Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery 15:332-339, 1984 17. Newton TH, Cronqvist S: Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 93:1071-1078, 1969 18. Obrador S, Soto M, Silvela J: Clinical syndromes of arteriovenous malformations of the transverse-sigmoid sinus. J Neurol Neurosurg Psychiatry 38:436-451, 1975 19. Pollock JA, Newton TH: The anterior falx artery: normal and pathologic anatomy. Radiology 91:1089-1095, 1968 20. Sundt TM Jr, Piepgras DG: The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 59:32-39, 1983 21. Symon L, Kuyama H, Kendall B: Dural arteriovenous malformations of the spine. Clinical features and surgical results in 55 cases. J Neurosurg 60:238-247, 1984 22. Terada T, Kikuchi H, Karasawa J, et al: Intracerebral arteriovenous malformation fed by the anterior ethmoidal artery: case report. Neurosurgery 14:578-582, 1984 23. Tiyaworabun S, Vonofakos D, Lorenz R: Intracerebral arteriovenous malformation fed by both ethomoidal arteries. Surg Neuroi 26:375-382, 1986 24. Vifiuela F, Fox AJ, Pelz DM, et al: Unusual clinical manifestations of dural arteriovenous malformations. J Neurosurg 64:554-558, 1986 25. Waga S, Fujimoto K, Morikawa A, et al: Dural arteriovenous malformation in the anterior fossa. Surg Neurol 8:356-358, 1977
Manuscript received August 8, 1989. Address reprint requests to." Neil Martin, M.D., Division of Neurosurgery, 74-140 CHS, University of California at Los Angeles Medical Center, Los Angeles, California 90024.