Mixed Pial-Dural Arteriovenous Malformation in the Anterior Cranial Fossa

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1 Neurol Med Chir (Tokyo) 50, , 2010 Mixed Pial-Dural Arteriovenous Malformation in the Anterior Cranial Fossa Two Case Reports Hiroyuki JIMBO, YukioIKEDA, HitoshiIZAWA, Kuninori OTSUKA, andjoharaoka* Department of Neurosurgery, Tokyo Medical University Hachioji Medical Center, Hachioji, Tokyo; *Department of Neurosurgery, Tokyo Medical University, Tokyo Abstract Most arteriovenous malformations (AVMs) associated with the meningeal artery in the anterior cranial fossa are the pure dural type, and mixed pial-dural AVMs are rare. Two types of mixed pial-dural AVM occur in the anterior cranial fossa according to the shunting point: one with the nidus in the brain parenchyma of the frontal lobe, and the other with the shunting point in the dura mater. We describe two patients with AVMs fed by the anterior ethmoidal arteries and the persistent primitive olfactory artery, with the nidus located in the pure brain parenchyma of the inferior aspect of frontal lobe, and drained via an abnormal cortical vein into the cavernous and superior sagittal sinuses. The importance of occluding the venous outflow to obliterate intracranial dural arteriovenous fistula (AVF) is emphasized. However, removal of the nidus in the brain parenchyma is required. The presence of a pial feeder should be considered before diagnosis of dural AVF of the anterior cranial fossa, and preoperative detailed evaluation for the pial supply and shunting point is mandatory. Key words: mixed pial-dural arteriovenous malformation, anterior cranial fossa, meningeal artery, pial artery, surgical resection Introduction Intracranial arteriovenous malformations (AVMs) can be classified on the basis of their arterial supply into pure pial, mixed pial-dural, and pure dural AVMs. 20) Dural arteriovenous fistulas (AVFs) are usually associated with venous hypertension due to sinus thrombosis, and frequently occur in the regions of the transverse and sigmoid sinuses. 2,9,10,15) Dural AVFs are now known to be entities distinct from AVMs. Pial AVMs are generally considered to be a developmental malformation, 18) whereas dural AVFs usually develop secondary to sinus thrombosis, trauma, and surgery. 2 4,9,10,15) The incidence of pure dural AVFs is lower in the anterior cranial fossa than in other parts of the brain, but the clinical characteristics have been clarified to some extent. 11,19,30) Mixed pial-dural AVM in the anterior cranial fossa is rare, with only 11 reported cases. 6,8,12,13,17,26,27,29,31 33) Two types of mixed pial-dural AVM occur in the anterior cranial fossa: one with the nidus in the brain parenchyma of the frontal lobe, and the other with the shunting point in the dura mater. We report two cases of mixed pial-dural AVM in the anterior cranial fossa with the nidus in the brain parenchyma. Received June 25, 2009; Accepted November 10, 2009 Case Reports Case 1: A 68-year-old man presented with severe headache and vomiting. He was hospitalized 2 hours after the onset of the symptoms and became comatose at the time of admission. Computed tomography (CT) revealed intracerebral hemorrhage in the left frontal base with ventricular rupture and acute hydrocephalus (Fig. 1). The patient underwent ventricular drainage, and gradually regained consciousness. Subsequently, angiography was performed. Three-dimensional (3D) digital subtraction angiography revealed a mixed pial-dural AVM fed by an anomalous left frontoorbital artery and the bilateral anterior ethmoidal arteries (AEAs). The malformation drained into the cavernous sinus via the dilated cortical vein and superior sagittal sinus (Figs. 2 and 3). The patient underwent bifrontal craniotomy 7 days after admission. Opening of the dura mater revealed several draining veins and a dilated venous sac on the surface of the frontal lobe. However, no drainage vein was recognized between the dura mater and the brain surface. Shunts from the anomalous frontoorbital artery on the brain surface, the AEA, and small arteries passing through the dura mater around the olfactory groove were observed and coagulated (Fig. 4). The nidus was located in the pure brain parenchyma of the inferior aspect of the frontal pole. Thereafter, the nidus with the venous sac on the surface was removed. 470

2 Mixed Pial-Dural AVM in the Anterior Cranial Fossa 471 Fig. 1 Case 1. Preoperative computed tomography scan showing intracerebral hemorrhage in the left frontal base with intraventricular hematoma and acute hydrocephalus. Fig. 4 Case 1. A: Intraoperative photograph showing the anterior ethmoidal artery (arrow) and the small meningeal artery (arrowhead) through the dura mater around the olfactory groove. The venous drainage between the dura mater and brain surface was not recognized. B: Intraoperative photograph showing the anomalous frontoorbital artery (arrow) asapial supply. Fig. 2 Case 1. A: Preoperative left carotid angiogram showing the arteriovenous malformation supplied by the left anterior ethmoidal artery (arrowhead), and the anomalous left frontoorbital artery (arrow). B: Preoperative three-dimensional angiogram showing the arteriovenous malformation supplied by the left anterior ethmoidal artery (arrowhead), and the anomalous left frontoorbital artery (arrow). Fig. 5 Case 1. Postoperative left carotid angiograms, anteroposterior (A) and lateral views (B), showing disappearance of the mixed pial-dural arteriovenous malformation in the anterior cranial fossa and vasospasm of the main arteries. Fig. 3 Case 1. A: Preoperative right carotid angiogram showing the arteriovenous malformation supplied by the right anterior ethmoidal artery. B, C: Preoperative left carotid angiogram showing the malformation drained into the cavernous sinus via the dilated cortical vein and superior sagittal sinus. Fig. 6 Case 1. Photomicrograph showing vessels of various sizes in the brain. Victoria blue hematoxylin and eosin stain, 20. Postoperative angiography showed no evidence of residual vascular malformations (Fig. 5). Histological examination revealed vessels of various sizes in the brain parenchyma and the diagnosis was AVM (Fig. 6). The postoperative course was uneventful. Complete recovery of the impaired higher cognitive functions was noted after the sur-

3 472 H. Jimbo et al. Fig. 7 Case 2. A: Preoperative computed tomography scan showing intracerebral hemorrhage in the left frontal base and subarachnoid hemorrhage. B: Three-dimensional computed tomography angiogram showing the arteriovenous malformation supplied by the anomalous left anterior ethmoidal artery (arrowhead) and persistent primitive olfactory artery (arrow). gery. Case 2: A 76-year-old man was hospitalized one hour after onset and became comatose. CT revealed left frontal base hemorrhage and subarachnoid hemorrhage (Fig. 7A). 3D CT angiography revealed a mixed pial-dural AVM fed by an anomalous left AEA and a pial artery originating from internal carotid artery as a persistent primitive olfactory artery (Fig. 7B). The malformation drained into the superior sagittal sinus via the dilated cortical vein. The patient underwent bifrontal craniotomy immediately and the nidus with venous sac was removed. The nidus was located in the brain parenchyma of the inferior aspect of the frontal lobe. No venous drainage between the dura mater and the brain surface was recognized. Postoperative magnetic resonance angiography found no evidence of residual malformations. The postoperative course was uneventful and he recovered consciousness. Discussion Table 1 shows the 13 patients including our two patients, of whom 11 were men with mean age of 61.8 years at onset. A new embryological classification of dural AVFs suggested that fistulas located in the lateral epidural space, which includes the lamina cribrosa ossis ethmoidalis, are strongly predominant in men, whereas those located in the ventral epidural space are more common in women. 5) Dural AVFs in the anterior cranial fossa occur predominantly in men. 24) Further, mixed pial-dural AVMs in the anterior cranial fossa also show the same level of male predominance. Most patients with mixed pial-dural AVMs in the anterior cranial fossa were symptomatic at the time of diagnosis (11 of 13). However, the lesion was discovered incidentally in the remaining 2 patients. Eight patients presented with intracranial hemorrhage, 1 patient with epilepsy, 1 patient with fourth nerve palsy, and 1 patient with pain in the forehead. TheAVMswerefedbytheAEAinall13patients:bythe ipsilateral AEA in 10 patients, and by the bilateral AEAs in the remaining 3. The AVMs were supplied by the external carotid arteries via branches of the middle meningeal artery, anterior falx artery, sphenopalatine artery, and superficial temporal artery in 3 of the 13 patients. The anomalous branches of the anterior cerebral artery in 8 patients and arterial supply from the internal carotid artery in one patient were found to supply blood to the nidus preoperatively. No pial arterial supply was found in the preoperative angiograms of 4 of the patients, but was found during the operation. 3D CT and 3D digital subtraction angiography are useful to evaluate the presence of pial supply as in our cases. The AVMs drained into the superior sagittal sinus through the pial vein in 10 patients, the cavernous sinus in 3, the transverse sinus in 1, and the straight sinus in 1. Venous pouches were present on the draining cortical vein in 11 of the 13 patients. The nidus was located in the brain parenchyma in 10 patients, in the dura mater in 2 patients, and the location was not described in 1 patient. The pathogenesis of mixed pial-dural AVMs in the anterior cranial fossa remains unclear. The presence of abnormal communications between the pial and meningeal arteries in the embryonic stage leads to the development of mixed pial-dural AVMs. 27) The anomalous, persistent primitiveolfactoryarterythatarisesfrombothinternal carotid artery and anterior cerebral artery has a connection with the ethmoidal artery. 21) However, pial arteries have an embryologic origin different from that of dural arteries, so the angiogenic mechanisms involved in the development of these two arterial systems may not necessarily be identical. 25) Venous hypertension occurring secondary to sinus thrombosis is believed to be the primary mechanism responsible for the formation of dural AVFs. 23) Venous hypertension may promote the growth of microscopic arteriovenous shunts, which are found within the vasa vasorum of normal pachymeninges, and may stimulate the release of angiogenic factors in experimental models. 7,14,15,28) Acquired pial AVMs may develop after sinus or cerebral venous thrombosis. 22) The mechanism causing these malformations originates in blocking of the communications between the cortical veins and dural sinuses as a result of retrograde thrombus propagation, resulting in increased cortical venous pressure, leading to the development of pial AVMs. 22) Thus, the occurrence of venous hypertension after venous obstruction, the expression of angiogenic factors, and other angiogenic mechanisms may lead to the development of both pial and dural malformations in the anterior cranial fossa. Twelve of the 13 patients were managed surgically by either frontal or bifrontal craniotomy, whereas the other patient was conservatively observed. Among the feeding arteries, the dural meningeal arteries were present in the cribriform plate, and the pial arteries were present either in the brain parenchyma or on the brain surface. The classification of AVM into pure dural, pure pial, and mixed pial-dural types depends on the blood supply and not the location of the shunting point. Two previous patients with mixed pial-dural AVM of the anterior cranial fossa had the shunting point in the dura mater. In this type, occlusion on the venous side adjacent to the shunt is sufficient. 16)

4 Mixed Pial-Dural AVM in the Anterior Cranial Fossa 473 Table 1 Summary of mixed pia-dural arteriovenous malformations in the anterior cranial fossa Case No. Author (Year) Age (yrs)/ Sex Clinical symptoms Location of nidus Feeding arteries Meningeal Pial Draining vein Vascular pouch Operation Outcome 1 Terada et al. (1984) 27) 64/F ICH cortex ipsi AEA frontal pial artery 2 Tiyaworabun et al. (1986) 29) 57/M ICH, SAH cortex bil AEAs ACA branches pial vein ª SSS, CS 3 Martin et al. (1990) 17) 48/M ICH dura (falx) ipsi AEA, STA SpV ª TS yes open surgery MD yes open surgery GR ACA branches pial vein ª SSS yes open surgery GR 4 Tanaka et al. (1991) 26) 60/M incidental parenchyma ipsi AEA FOA pial vein ª SSS yes open surgery GR FOA FOV, OV, RoV yes open surgery GR 5 Yamamoto et al. (1993) 31) 62/M IVth nerve palsy dura, olfactory bulb ipsi AEA, ipsi MMA, bil AFAs 6 Yoshida and 51/M ICH parenchyma bil AEAs ACA branches pial vein ª Yamamoto (1993) 32) dural vein yes open surgery GR 7 Yoshimoto et al. (1993) 33) 66/M ICH cortex ipsi AEA FBA pial vein ª SSS yes open surgery GR 8 Hashimoto et al. (1996) 8) 65/M epilepsy cortex ipsi AEA FPA pial vein ª SSS no open surgery GR 9 Gliemroth et al. (1999) 6) 69/F ICH, IVH cortex ipsi AEA FPA SSS yes open surgery SD 10 Kawaguchi et al. (1999) 13) 60/M headache not described ipsi AEA, ACA branches SSS, CS no conservative not ipsi STA, described ipsi MMA 11 Kanai et al. (2000) 12) 57/M incidental cortex ipsi AEA FOA pial vein ª SSS yes open surgery GR 12 Present Case 1 68/M ICH, IVH cortex bil AEAs FOA pial vein ª CS, SSS yes open surgery GR 13 Present Case 2 76/M ICH, SAH cortex ipsi AEA PPOA pial vein ª SSS yes open surgery MD ACA: anterior cerebral artery, AEA: anterior ethmoidal artery, AFA: anterior falcian artery, CS: cavernous sinus, FBA: frontobasal artery, FOA: frontoorbital artery, FOV: frontoorbital vein, FPA: frontopolar artery, GR: good recovery, ICH: intracranial hemorrhage, IVH: intraventricular hemorrhage, MD: moderate disability, MMA: middle meningeal artery, OV: olfactory vein, PPOA: persistent primitive olfactory artery, RoV: Rosenthal vein, SAH: subarachnoid hemorrhage, SD: severe disability, SpV: sphenopetrosal vein, SSS: superior sagittal sinus, STA: superficial temporal artery, TS: transverse sinus.

5 474 H. Jimbo et al. However,inthetypewiththenidusinthebrainparenchyma, removal of the nidus with/without the venous sac is necessary. The outcome was favorable in 11 of the 13 patients (good recovery in 9 patients, and moderate disability in 2). One patient showed severe disability, and the outcome was not reported for the other patient. Surgical resection is the most reliable procedure for the treatment of mixed pial-dural AVMs in the anterior cranial fossa. However, a low-risk procedure has recently been developed involving disconnection of pure dural AVF in the anterior cranial fossa by injecting N-butyl cyanoacrylate through the ophthalmic artery. 1) Further, the limited space in open surgery makes the meningeal feeding arteries around the cribriform plate difficult to identify and ligate. Therefore, a combination of endovascular embolization and open surgery is a possible therapeutic option. 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6 475 28) TeradaT,TsuuraM,KomaiN,HigashidaRT,HalbachVV, Dowd CF, Wilson CB, Hieshima GB: The role of angiogenic factor bfgf in the development of dural AVFs. Acta Neurochir (Wien) 138: , ) Tiyaworabun S, Vonofakos D, Lorez R: Intracerebral arteriovenous malformation fed by both ethmoidal arteries. Surg Neurol 26: , ) XavierJ,CruzR,StockerA,VasconcelosC,ReisJ,Almeida- Pinto J: [Dural fistulas of the anterior cranial fossa]. Acta Med Port 14: 71 75, 2001 (Por) 31) Yamamoto M, Fukushima T, Sakamoto S, Hashimoto T, Tomonaga M, Goto K: [Isolated trochlear nerve palsy caused by mixed dural-pial arteriovenous malformation of the anterior cranial fossa: A case report]. No Shinkei Geka 21: , 1993 (Jpn) 32) Yoshida S, Yamamoto T: Intracerebral arteriovenous malformations supplied by ethmoidal arteries: Case report. Neurol Med Chir (Tokyo) 33: , ) YoshimotoH,YukawaO,AoyamaH,MaedaH,UozumiT: Intracerebral arteriovenous malformation fed by the anterior ethmoidal artery: Case report. Neurol Med Chir (Tokyo) 33: , 1993 Address reprint requests to: Hiroyuki Jimbo, M.D., Department of Neurosurgery, Tokyo Medical University Hachioji Medical Center, 1163 Tate machi, Hachioji, Tokyo , Japan. hjimbo@tokyo-med.ac.jp