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Surgical treatment of intracranial dural arteriovenous fistulas
Vascular
Surgical Treatment of Intracranial Dural Arteriovenous Fistulas Satoshi Ushikoshi,* Kiyohiro Houkin,† Satoshi Kuroda,† Takeshi Asano,* Yoshinobu Iwasaki,† Kazuo Miyasaka,* and Hiroshi Abe† *Department of Radiology and †Neurosurgery, Hokkaido University School of Medicine, Sapporo, Japan
Ushikoshi S, Houkin K, Kuroda S, Asano T, Iwasaki Y, Miyasaka K, Abe H. Surgical treatment of intracranial dural arteriovenous fistulas. Surg Neurol 2002;57:253– 61.
KEY WORDS
Intracranial dural arteriovenous fistula, endovascular treatment, surgery.
BACKGROUND
When considering the treatment strategies for dural arteriovenous fistulas (DAVFs), it is important to clarify the exact location of the fistula and venous drainage route from both DAVFs and normal brain tissue. DAVFs with leptomeningeal retrograde venous drainage carry a high risk of neurological deficits and require aggressive treatment. When AVFs involve the dural sinus, transvenous embolization via the transfemoral approach is usually the first choice of treatment. For DAVFs draining directly into the cortical veins without dural sinus involvement, transarterial embolization may be a curative treatment. However, when embolization is technically difficult or results in incomplete occlusion, surgical treatment is required. The purpose of the present study was to review our experience with surgical treatment of DAVFs. METHODS
The present series included 17 patients; 9 had DAVFs involving the dural sinus with leptomeningeal retrograde venous drainage and 8 had DAVFs draining directly into the cortical veins. For DAVFs involving the sinus, embolization of the diseased sinus by direct surgical exposure was performed in 8 patients, and surgical excision in one. For DAVFs draining directly into the cortical veins, interruption of the draining veins close to DAVFs was undertaken in 7 and surgical excision in 1. RESULTS
Complete obliteration of DAVFs was demonstrated in 16 patients. At final follow-up, 15 patients were asymptomatic and the other 2 showed clinical improvement. CONCLUSIONS
For DAVFs involving the dural sinus, direct operative sinus packing is indicated. For DAVFs directly draining into the cortical veins, surgical interruption of the draining veins is indicated. © 2002 by Elsevier Science Inc.
Address reprint requests to: Satoshi Ushikoshi, Department of Radiology, Hokkaido University School of Medicine, Kita 15 jyou Nishi 7 Choume, Kitaku, Sapporo Japan. Received December 6, 2000; accepted September 24, 2001. © 2002 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
ural arteriovenous fistulas (DAVFs) with leptomeningeal retrograde venous drainage carry a high risk of intracranial hemorrhage or neurological deficits, and require aggressive treatment to achieve complete obliteration of the lesions [2,3, 5,7,14]. Transvenous embolization via the transfemoral approach is the first choice of treatment, and has a high cure rate [11,16,19]. However, the percutaneous transvenous approach to the fistula is sometimes impossible because of severe stenosis or bifocal occlusion of the sinus. Transarterial embolization using liquid embolic materials is another option, but complete obliteration rates are considerably lower [1,11,19]. In such patients, surgical treatment is indicated. In the present study, we retrospectively evaluated the results of surgical treatment of intracranial DAVFs.
D
Materials and Methods The subjects were 17 patients with intracranial DAVFs who underwent surgical treatment. The patients ranged in age from 31 to 74 years (mean 60 years), and there were 13 men and 4 women. Clinical symptoms and imaging findings are summarized in Table 1. These 17 patients were classified into two groups based on the anatomic features: (1) DAVFs with cortical venous drainage alone (without dural sinus involvement); (2) AVFs involving the dural sinus with retrograde leptomeningeal venous drainage. 0090-3019/02/$–see front matter PII S0090-3019(02)00641-9
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Direct sinus packing was performed in 8 patients. The diseased segment of the dural sinus was exposed and an 18-gauge elastic needle was inserted into it. The diseased sinus was packed as tightly as possible with large fibered occlusion coils (0.035 or 0.038 in) under the guidance of intraoperative digital subtraction angiography (DSA) (Figure 3). In one patient with a DAVF of the confluence of sinuses, the microcatheter was advanced into the diseased segment of the sinus through the 18-gauge needle, and interlocking detachable coils and fibered platinum coils (0.018 in) were used for packing the sinus (Figure 3). In 1 patient with a DAVF of the superior sagittal sinus, the diseased segment of the sinus was excised (Figure 4). Lesion localization was aided by intraoperative DSA. Special attention was paid to not interrupting the cortical veins that contributed to the venous drainage of normal brain tissue.
SURGICAL PROCEDURES.
Clinical Symptoms and Imaging Findings
FINDING
NO. OF PATIENTS
Consciousness disturbance Dementia Seizure Aphasia Hemimparesis Papilledema Myelopathy Headache Tinnitus Dizziness Intracerebral hemorrhage Brain swelling, venous infarction
2 1 4 2 1 1 1 3 3 1 5 6
DAVF WITH CORTICAL VENOUS DRAINAGE ALONE Eight patients were classified as this type. These DAVFs were located in the posterior cranial fossa in 2 patients, frontal lobe in 2, occipital lobe in 1, and temporal lobe in 3. PREOPERATIVE EMBOLIZATION. Transarterial embolization was performed in four patients before surgery. In 1 patient, polyvinyl alcohol (PVA) particles were used as an embolic material to reduce the shunted blood flow. In 3 patients, a microcatheter could be advanced close to the fistula and N-butylcyanoacrylate (NBCA) was used to attempt complete obliteration (Figure 1).
In 7 patients, surgical management consisted of interruption of the draining vein as close as possible to the DAVF (Figure 1). In 1 patient, the affected dura was excised completely (Figure 2).
SURGICAL PROCEDURES.
AVF INVOLVING THE DURAL SINUS WITH LEPTOMENINGEAL RETROGRADE VENOUS DRAINAGE Nine patients were classified as this type. These DAVFs were located in the superior sagittal sinus in 1 patient, transverse-sigmoid sinus in 7, and multiple dural sinuses in 1 patient (superior sagittal sinus and confluence of sinuses). Surgical treatment was preceded by transarterial embolization in 8 patients. PVA particles were used in all patients to reduce the arterial inflow and facilitate the operative exposure of the involved dural sinuses. In 1 patient, NBCA was also used to attempt complete obliteration (Figure 3).
PREOPERATIVE EMBOLIZATION.
Illustrative Cases CASE 1 In this 61-year-old woman, a DAVF was diagnosed incidentally; she presented with no neurological symptoms caused by this lesion (Figure 1). Angiography revealed the DAVF directly emptying into the right occipital cortical vein. The right middle meningeal artery was catheterized as close to the AVF as possible and embolization with NBCA was performed. However, NBCA did not penetrate the fistula sufficiently, and the right external carotid angiogram after the embolization revealed persistent filling of the fistula. She underwent surgical interruption of the draining vein close to the fistula and complete obliteration was achieved. CASE 2 This 71-year-old woman presented with pulsatile tinnitus and retroauricular pain on the left side (Figure 2). Angiography demonstrated a DAVF at the origin of the vein of Labbe, which showed varicose dilatation, and both retrograde and antegrade venous drainage were noted. The transfemoral venous approach to the fistulous portion appeared possible; however, it was thought that tight packing to obtain complete occlusion of this high-flow lesion would be difficult. When the AVF did not occlude completely, diversion of the shunted blood flow to the cortical vein would occur and the venous hypertension would worsen. Therefore, we decided to perform surgery. She underwent transarterial embolization using PVA particles, followed by craniotomy. First, all the cortical venous outlets
Surgical Treatment of DAVFs
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Case 1: right external carotid angiogram, anteroposterior projection (A) and lateral projection (B), showing a dural arteriovenous fistula draining directly into an occipital cortical vein. (C) selective injection of the right middle meningeal artery. (D) Right external carotid angiogram after the embolization, lateral projection, showing persistent filling of the fistula.
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were interrupted as close to the fistula as possible, and then the diseased dura matter was excised completely with the varix. The postoperative course was uneventful and angiography revealed the complete disappearance of the DAVF and preservation of the left transverse sinus. CASE 3 This 69-year-old man presented with rapidly progressive dementia (Figure 3). Angiography showed multiple DAVFs involving the superior sagittal sinus and the confluence of the sinuses. The bilateral transverse sinuses and superior sagittal sinus distal to the fistula were occluded and retrograde venous drainage was prominent. Bilateral external carotid branches were extensively embolized using PVA particles and NBCA. Angiography after transarterial embolization demonstrated persistent filling of the
fistulas, although the shunted blood flow was significantly reduced. He underwent intraoperative direct sinus packing. A postoperative angiography showed complete obliteration of both lesions, and the neurological symptoms also completely resolved. CASE 4 This 40-year-old man presented with papilledema and increased intracranial pressure (Figure 4). Angiography showed a DAVF of the superior sagittal sinus with leptomeningeal retrograde venous drainage and venous congestion of the bilateral cerebral hemispheres. The diseased sinus did not contribute to the venous drainage of the surrounding normal brain. First, a transfemoral venous approach to the diseased sinus was attempted but failed because of severe stenosis of the superior sagittal sinus proximal to the AVF. A cortical vein, draining the normal
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Case 2: left external carotid angiogram, arterial (A) and venous phase (B), and left occipital angiogram, lateral projection (C), showing a dural arteriovenous fistula (DAVF) at the origin of the vein of Labbe. Both retrograde and antegrade venous drainage were noted. (D) Postoperative left common carotid angiogram, lateral projection, showing complete disappearance of the DAVF. (E) Right internal carotid angiogram, venous phase, anteroposterior projection, showing the preserved left transeverse sinus.
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brain, went into the superior sagittal sinus just posterior to the AVF and it appeared difficult to occlude the AVF selectively, preserving this important cortical vein, under the guidance of intraoperative DSA. He underwent surgical excision. However, it was difficult to localize the lesion precisely and to differentiate the cortical veins with retrograde filling of the shunted blood flow from those draining the normal surrounding brain, and a postoperative angiogram showed small residual fistulas with retrograde venous drainage. However, the venous return from both cerebral hemispheres improved and symptoms of increased intracranial pressure were significantly reduced.
Results ANATOMIC RESULTS In 16 patients, postoperative angiography revealed complete disappearance of the DAVF. In one patient who underwent direct sinus packing for a DAVF of
the transverse sinus, intraoperative DSA after the packing was completed demonstrated persistent filling of the fistula draining into the vein of Labbe. Therefore, interruption of the vein of Labbe was performed, and postoperative angiography revealed no residual filling of the fistula. In 1 patient who underwent surgical excision of the diseased segment of the sinus, small residual fistulas were demonstrated on postoperative angiography (Figure 4). CLINICAL RESULTS Fourteen patients were clinically asymptomatic at final follow-up. The other 3 patients—2 presenting with aphasia caused by intracerebral hemorrhage and 1 presenting with consciousness disturbance (semicoma) caused by diffuse brain swelling— experienced significant clinical improvements after the treatment; however, mild aphasia and memory disturbances, respectively, remained. There were no treatment-related complications.
Surgical Treatment of DAVFs
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Case 3: left external carotid angiogram, anteroposterior projection (A), lateral projection arterial phase (B), and venous phase (C), showing multiple DAVFs involving the superior sagittal sinus and the confluence of the sinuses. Bilateral transverse sinuses and superior sagittal sinus distal to the fistula were occluded and retrograde venous drainage was prominent. (D) Left external carotid angiogram, lateral projection, after the transarterial embolization showing significant reduction of the shunted blood flow. (E) Skull X-ray film after direct sinus packing, lateral projection, showing the coils in the affected sinuses. (F) Postoperative left common carotid angiogram, lateral projection, showing complete obliteration of both DAVFs.
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Discussion In patients with intracranial DAVFs, the most important factor that determines the clinical presentation and prognosis is restrictive change of venous out-
flow and venous drainage pattern [2,3,5,7,14]. To predict the clinical presentation and to guide therapeutic decision-making, several classifications of DAVFs have been developed considering these factors [2,5,14]. When the fistulas are drained only
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Case 4: left external carotid angiogram, anteroposterior projection (A) and lateral projection (B), showing a DAVF involving the superior sagittal sinus with leptomeningeal retrograde venous drainage. (C) Left external carotid angiogram, arterial phase oblique projection, showing the precise location of the DAVF (arrowheads). (D) Internal carotid angiogram, venous phase oblique projection, showing that the diseased sinus did not contribute to the venous drainage of the surrounding the normal brain and normal cortical vein went into the superior sagittal sinus just posterior to the DAVF. Arrow and curved arrow indicate the direction of the venous blood flow. (E) Postoperative right common carotid angiogram, lateral projection, showing a small residual DAVF with retrogade venous drainage (small arrows).
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through the sinus antegradely, they are usually asymptomatic and exhibit benign courses. In this type of DAVF, aggressive treatment such as transvenous embolization or surgical resection is not indicated because of the risks of venous infarction caused by occluding the venous drainage from normal brain tissue. On the other hand, when the fistulas have retro-
grade leptomeningeal venous drainage, they are associated with aggressive clinical behavior and require aggressive treatment. The goal of treatment is complete occlusion or at least conversion of a highrisk type to a low-risk type by eliminating the retrograde leptomeningeal drainage. Usually, in DAVFs with retrograde leptomeningeal venous drainage, these veins do not contribute to the venous drain-
Surgical Treatment of DAVFs
age from the normal brain tissue any more, and occlusion of the venous side of the fistula can be performed without risk of venous infarction. Therefore, percutaneous transvenous embolization is widely accepted as the first choice of treatment because of the lower invasiveness and high cure rate [11,16,19]. However, severe stenosis or bifocal occlusion of the venous outlet are not uncommon findings in these high-risk DAVFs, and make the percutaneous transvenous approach to the fistula difficult. In these situations, surgical interventions are required. Recent reports of histopathological examinations of DAVFs suggest that the essential lesion was direct communication between dural arteries and dural veins within the dural sinus wall, not a direct fistula between the arteries and the dural sinus [12,15]. The venous outflow may drain into the adjacent sinus or cortical veins. Surgical strategies should be chosen considering the angioarchitecture, especially the direction of venous drainage from the fistula. We simply classified the DAVFs into the following two subtypes based on the angiographical findings: (1) DAVFs with cortical venous drainage alone; (2) AVFs involving the dural sinus with leptomeningeal retrograde venous drainage. DAVFS WITH CORTICAL VENOUS DRAINAGE ALONE The angioarchitecture of this DAVF type is relatively simple, and surgical treatment is technically easy and safe [6,13,18]. When the venous drainage goes into the cortical vein retrogradely and there is no antegrade venous outflow into the neighboring sinus, complete and permanent obliteration can be achieved by simple interruption of the draining vein as close to the fistula as possible without excision of the AVF. This procedure can be performed via a small craniotomy and with minimal invasion of the brain. The present study included 8 patients with DAVFs with cortical venous drainage alone. In 1 patient, there was a large varix at the fistulous point and antegrade flow from this varix toward the sinus was also noted. Therefore, complete excision of the varix was performed in this patient. The other 7 patients underwent simple interruption of the draining vein and complete obliteration of the DAVF was achieved without any complications in all patients. When antegrade venous outflow into the sinus is also noted, it is important to differentiate this subgroup of DAVFs from those involving the dural sinus with retrograde leptomeningeal venous drainage. In Case 2, there was a large varix at the fistulous point, and antegrade flow from this varix
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toward the transverse sinus was also noted. Therefore, complete excision of the varix, preserving the patency of the transverse sinus, was performed in this patient. If it is misdiagnosed as a DAVF involving the sinus and occlusion or resection of the sinus is performed, it may result in worsening of the venous hypertension. When there is an arterial pedicle through which the microcatheter can be navigated close to the fistula, transarterial embolization with NBCA may provide complete obliteration of the lesion by penetrating distally to the proximal portion of the draining vein [1,5]. Because this is less invasive, transarterial embolization with NBCA may be used as the first choice of treatment, although the cure rate is not high. When the main arterial pedicles originate from the internal carotid or vertebral artery, or when the risk of occlusion of nutrient vessels of cranial nerves is high, transarterial embolization using NBCA should not be undertaken. Recent advancements in microcatheters and coils enable percutaneous transvenous embolization in this DAVF type in some specific cases [4, 8]. However, navigation of the microcatheter via the tortuous cortical vein is extremely hazardous and it should not be performed as the first choice of treatment. AVFS INVOLVING THE DURAL SINUS WITH RETROGRADE LEPTOMENINGEAL VENOUS DRAINAGE Usually, there are multiple small arterial pedicles and complete obliteration of the fistula by transarterial embolization alone is difficult [11,19]. The value of transarterial embolization preceding the curative treatment is controversial. It is suggested that particulate embolization is safe and effective to reduce the shunted blood flow and to facilitate subsequent transvenous embolization or surgery [6,10]. Moreover, superselective angiography may provide important information about the precise location of the lesion. The previously reported surgical procedure was as follows [6,17]: the affected dural sinus was exposed widely, the dura was incised on each side of the sinus until it was isolated completely, all the efferent arterialized veins were cut, and the sinus was ligated proximally and distally and removed. This is a more tedious procedure that may result in intradural complications and tremendous blood loss [17]. We performed surgical excision of the DAVF in only one patient with a superior sagittal sinus lesion (Figure 4). In this patient, it was difficult to localize the lesion precisely and to differentiate
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the cortical veins with retrograde filling of the shunted blood flow from those draining the normal surrounding brain. Therefore, the extent of the excision was insufficient and postoperative DSA revealed minimal persistent filling of the fistula. Transvenous embolization plays a key role in the curative treatment of AVFs involving the dural sinus [11,16,19]. When transfemoral venous access is difficult because of severe stenosis or bifocal occlusion of the sinus, intraoperative direct sinus packing is technically easy and effective, and is considered the first choice of treatment [9 –11,19]. Complete cure is not always achieved by transvenous embolization or direct sinus packing [10,11, 19], and some studies have emphasized the superiority of the surgical excision because of its high cure rate [6]. However, it is suggested that when intra- or postoperative control angiography reveals persistent filling of the fistula after the packing is completed, a complementary surgical excision or interruption of the draining vein should be performed [10]. This procedure can be performed more easily and safely after significant reduction of shunted blood flow by sinus packing compared with direct surgical excision without sinus packing. Endo et al suggest that a small craniotomy or burr hole is enough for direct sinus packing [9]. We prefer to expose the affected sinus widely. There is a possible subtype of DAVF involving both the dural sinus and cortical veins and it is sometimes difficult to differentiate this type from DAVFs involving only the dural sinus by preoperative examinations. In this subtype, occlusion of the sinus alone may result in persistent filling of the AVF with cortical venous drainage alone. In this situation, subsequent surgical procedures to occlude this remnant can be performed more easily through the wide operative field.
Conclusion 1. For high-risk DAVFs with leptomeningeal retrograde venous drainage, when embolization is technically difficult or has resulted in incomplete occlusion, surgical treatment is indicated. 2. When considering surgical strategies, it is essential to evaluate the precise location of the AVF, the anatomic features, and venous drainage from both the AVF and normal brain. 3. DAVFs with cortical venous drainage alone without dural sinus involvement are best treated by interruption of the draining vein close to the fistula. 4. AVFs involving the dural sinus with retrograde
Ushikoshi et al
leptomeningeal venous drainage can be treated by transarterial embolization combined with direct tight packing of the diseased sinus for a high rate of cure and a low rate of morbidity. REFERENCES 1. Barnwell SL, Halbach VV, Dowd CF, Higashida RT, Hieshima GB, Wilson CB. A variant of arteriovenous fistulas within the wall of dural sinuses. Results of combined surgical and endovascular therapy. J Neurosurg 1991;74:199 –204. 2. Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 1995;82:166 –79. 3. Brown RD, Wiebers DO, Nichols DA. Intracranial dural arteriovenous fistulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 1994;81:531– 8. 4. Cloft HJ, Kallmes DF, Jensen ME, Dion JE. Percutaneous transvenous coil embolization of a Type 4 sagittal sinus dural arteriovenous fistula: case report. Neurosurgery 1997;41:1191– 4. 5. Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, Chiras J, Merland JJ. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 1995;194:671– 80. 6. Collice M, D’Aliberti G, Arena O, Solaini C, Fontana RA, Talamonti G. Surgical treatment of intracranial dural arteriovenous fistulae: role of venous drainage. Neurosurgery 2000;47:56 – 67. 7. Davies MA, TerBrugge K, Willinsky R, Coyne T, Saleh J, Wallace C. The Validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 1996;85:830 –7. 8. Defreyne L, Valangenhove P, Vandekerckhove T, Deschrijver I, Sieben G, Klaes R, Kunnen M. Transvenous embolization of a dural arteriovenous fistula of the anterior cranial fossa: Preliminary results. Am J Neuroradiol 2000;21:761–5. 9. Endo S, Kuwayama N, Takaku A, Nishijima M. Direct packing of the isolated sinus in patients with dural arteriovenous fistulas of the transverse-sigmoid sinus. J Neurosurg 1998;88:449 –56. 10. Goto K, Sidipratomo P, Ogata N, Inoue T, Matsuno H. Combining endovascular and neurosurgical treatments of high-risk dural arteriovenous fistulas in the lateral sinus and the confluence of the sinuses. J Neurosurg 1999;90:289 –99. 11. Halbach VV, Higashida RT, Hieshima GB, Mehringer CM, Hardin CW. Transvenous embolization of dural fistulas involving the transverse and sigmoid sinuses. Am J Neuroradiol 1989;10:385–92. 12. Hamada Y, Goto K, Inoue T, Iwaki T, Matsuno H, Suzuki S, Matsushima T, Fukui M, Miyake E. Histopathological aspects of dural arteriovenous fistulas in the transverse-sigmoid sinus region in nine patients. Neurosurgery 1997;40:452– 8. 13. Hoh BL, Choudhri TF, Connolly Jr ES, Solomon RA. Surgical management of high-grade intracranial dural arteriovenous fistulas: leptomeningeal venous disruption without nidus excision. Neurosurgery 1998; 42:796 – 805.
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14. Lalwani AK, Dowd CF, Halbach VV. Grading venous restrictive disease in patients with dural arteriovenous fistulas of the transverse/sigmoid sinus. J Neurosurg 1993;79:11–5. 15. Nishijima M, Takaku A, Endo S, Kuwayama N, Koizumi F, Sato H, Owada K. Etiological evaluation of dural arteriovenous malformations of the lateral and sigmoid sinuses based on histopathological examinations. J Neurosurg 1992;76:600 – 6. 16. Roy D, Raymond J. The role of transvenous embolization in the treatment of intracranial dural arteriovenous fistulas. Neurosurgery 1997;40:1133– 44. 17. Sundt TM, Piepgras DG. The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 1983;59:32–9. 18. Thompson BG, Doppman JL, Oldfield EH. Treatment of cranial dural arteriovenous fistulae by interruption of leptomeningeal venous drainage. J Neurosurg 1994; 80:617–23. 19. Urtasun F, Biondi A, Casasco A, Houdart E, Caputo N, Aymard A, Merland JJ. Cerebral dural arteriovenous fistulas: percutaneous transvenous embolization. Radiology 1996;199:209 –17.
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COMMENTARY
Ushikoshi and co-authors have collected a series of cases of dural fistulas associated with cortical venous drainage. There is no doubt that this is a subgroup of dural fistulas that puts the patient at risk of intraparenchymal hemorrhage or infarctions. Therefore, these patients must be treated aggressively. The authors have succeeded in curing this difficult-to-treat condition with a combination of embolization and surgical exposure. At surgery, they either resected the sinus, packed it with coils, or ligated the arterialized vein at the fistula level. They should be congratulated on their results. The progress in the development and navigation of microcatheters will continue to increase the number of these cases that can be cured with embolization alone. Gerard Debrun, M.D. Interventional Neuroradiologist Paris, France
hen I stand before God at the end of my life, I would hope that I would not have a single bit of talent left, and could say “I used everything you gave me.”
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—Erma Bombeck
n every outthrust headland, in every curving beach, in every grain of sand there is the story of the earth.
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—Rachel Carson
Surgical Treatment of Intracranial Dural Arteriovenous Fistulas Satoshi Ushikoshi,* Kiyohiro Houkin,† Satoshi Kuroda,† Takeshi Asano,* Yoshinobu Iwasaki,† Kazuo Miyasaka,* and Hiroshi Abe† *Department of Radiology and †Neurosurgery, Hokkaido University School of Medicine, Sapporo, Japan
Ushikoshi S, Houkin K, Kuroda S, Asano T, Iwasaki Y, Miyasaka K, Abe H. Surgical treatment of intracranial dural arteriovenous fistulas. Surg Neurol 2002;57:253– 61.
KEY WORDS
Intracranial dural arteriovenous fistula, endovascular treatment, surgery.
BACKGROUND
When considering the treatment strategies for dural arteriovenous fistulas (DAVFs), it is important to clarify the exact location of the fistula and venous drainage route from both DAVFs and normal brain tissue. DAVFs with leptomeningeal retrograde venous drainage carry a high risk of neurological deficits and require aggressive treatment. When AVFs involve the dural sinus, transvenous embolization via the transfemoral approach is usually the first choice of treatment. For DAVFs draining directly into the cortical veins without dural sinus involvement, transarterial embolization may be a curative treatment. However, when embolization is technically difficult or results in incomplete occlusion, surgical treatment is required. The purpose of the present study was to review our experience with surgical treatment of DAVFs. METHODS
The present series included 17 patients; 9 had DAVFs involving the dural sinus with leptomeningeal retrograde venous drainage and 8 had DAVFs draining directly into the cortical veins. For DAVFs involving the sinus, embolization of the diseased sinus by direct surgical exposure was performed in 8 patients, and surgical excision in one. For DAVFs draining directly into the cortical veins, interruption of the draining veins close to DAVFs was undertaken in 7 and surgical excision in 1. RESULTS
Complete obliteration of DAVFs was demonstrated in 16 patients. At final follow-up, 15 patients were asymptomatic and the other 2 showed clinical improvement. CONCLUSIONS
For DAVFs involving the dural sinus, direct operative sinus packing is indicated. For DAVFs directly draining into the cortical veins, surgical interruption of the draining veins is indicated. © 2002 by Elsevier Science Inc.
Address reprint requests to: Satoshi Ushikoshi, Department of Radiology, Hokkaido University School of Medicine, Kita 15 jyou Nishi 7 Choume, Kitaku, Sapporo Japan. Received December 6, 2000; accepted September 24, 2001. © 2002 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
ural arteriovenous fistulas (DAVFs) with leptomeningeal retrograde venous drainage carry a high risk of intracranial hemorrhage or neurological deficits, and require aggressive treatment to achieve complete obliteration of the lesions [2,3, 5,7,14]. Transvenous embolization via the transfemoral approach is the first choice of treatment, and has a high cure rate [11,16,19]. However, the percutaneous transvenous approach to the fistula is sometimes impossible because of severe stenosis or bifocal occlusion of the sinus. Transarterial embolization using liquid embolic materials is another option, but complete obliteration rates are considerably lower [1,11,19]. In such patients, surgical treatment is indicated. In the present study, we retrospectively evaluated the results of surgical treatment of intracranial DAVFs.
D
Materials and Methods The subjects were 17 patients with intracranial DAVFs who underwent surgical treatment. The patients ranged in age from 31 to 74 years (mean 60 years), and there were 13 men and 4 women. Clinical symptoms and imaging findings are summarized in Table 1. These 17 patients were classified into two groups based on the anatomic features: (1) DAVFs with cortical venous drainage alone (without dural sinus involvement); (2) AVFs involving the dural sinus with retrograde leptomeningeal venous drainage. 0090-3019/02/$–see front matter PII S0090-3019(02)00641-9
254 Surg Neurol 2002;57:253–61
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Direct sinus packing was performed in 8 patients. The diseased segment of the dural sinus was exposed and an 18-gauge elastic needle was inserted into it. The diseased sinus was packed as tightly as possible with large fibered occlusion coils (0.035 or 0.038 in) under the guidance of intraoperative digital subtraction angiography (DSA) (Figure 3). In one patient with a DAVF of the confluence of sinuses, the microcatheter was advanced into the diseased segment of the sinus through the 18-gauge needle, and interlocking detachable coils and fibered platinum coils (0.018 in) were used for packing the sinus (Figure 3). In 1 patient with a DAVF of the superior sagittal sinus, the diseased segment of the sinus was excised (Figure 4). Lesion localization was aided by intraoperative DSA. Special attention was paid to not interrupting the cortical veins that contributed to the venous drainage of normal brain tissue.
SURGICAL PROCEDURES.
Clinical Symptoms and Imaging Findings
FINDING
NO. OF PATIENTS
Consciousness disturbance Dementia Seizure Aphasia Hemimparesis Papilledema Myelopathy Headache Tinnitus Dizziness Intracerebral hemorrhage Brain swelling, venous infarction
2 1 4 2 1 1 1 3 3 1 5 6
DAVF WITH CORTICAL VENOUS DRAINAGE ALONE Eight patients were classified as this type. These DAVFs were located in the posterior cranial fossa in 2 patients, frontal lobe in 2, occipital lobe in 1, and temporal lobe in 3. PREOPERATIVE EMBOLIZATION. Transarterial embolization was performed in four patients before surgery. In 1 patient, polyvinyl alcohol (PVA) particles were used as an embolic material to reduce the shunted blood flow. In 3 patients, a microcatheter could be advanced close to the fistula and N-butylcyanoacrylate (NBCA) was used to attempt complete obliteration (Figure 1).
In 7 patients, surgical management consisted of interruption of the draining vein as close as possible to the DAVF (Figure 1). In 1 patient, the affected dura was excised completely (Figure 2).
SURGICAL PROCEDURES.
AVF INVOLVING THE DURAL SINUS WITH LEPTOMENINGEAL RETROGRADE VENOUS DRAINAGE Nine patients were classified as this type. These DAVFs were located in the superior sagittal sinus in 1 patient, transverse-sigmoid sinus in 7, and multiple dural sinuses in 1 patient (superior sagittal sinus and confluence of sinuses). Surgical treatment was preceded by transarterial embolization in 8 patients. PVA particles were used in all patients to reduce the arterial inflow and facilitate the operative exposure of the involved dural sinuses. In 1 patient, NBCA was also used to attempt complete obliteration (Figure 3).
PREOPERATIVE EMBOLIZATION.
Illustrative Cases CASE 1 In this 61-year-old woman, a DAVF was diagnosed incidentally; she presented with no neurological symptoms caused by this lesion (Figure 1). Angiography revealed the DAVF directly emptying into the right occipital cortical vein. The right middle meningeal artery was catheterized as close to the AVF as possible and embolization with NBCA was performed. However, NBCA did not penetrate the fistula sufficiently, and the right external carotid angiogram after the embolization revealed persistent filling of the fistula. She underwent surgical interruption of the draining vein close to the fistula and complete obliteration was achieved. CASE 2 This 71-year-old woman presented with pulsatile tinnitus and retroauricular pain on the left side (Figure 2). Angiography demonstrated a DAVF at the origin of the vein of Labbe, which showed varicose dilatation, and both retrograde and antegrade venous drainage were noted. The transfemoral venous approach to the fistulous portion appeared possible; however, it was thought that tight packing to obtain complete occlusion of this high-flow lesion would be difficult. When the AVF did not occlude completely, diversion of the shunted blood flow to the cortical vein would occur and the venous hypertension would worsen. Therefore, we decided to perform surgery. She underwent transarterial embolization using PVA particles, followed by craniotomy. First, all the cortical venous outlets
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Case 1: right external carotid angiogram, anteroposterior projection (A) and lateral projection (B), showing a dural arteriovenous fistula draining directly into an occipital cortical vein. (C) selective injection of the right middle meningeal artery. (D) Right external carotid angiogram after the embolization, lateral projection, showing persistent filling of the fistula.
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were interrupted as close to the fistula as possible, and then the diseased dura matter was excised completely with the varix. The postoperative course was uneventful and angiography revealed the complete disappearance of the DAVF and preservation of the left transverse sinus. CASE 3 This 69-year-old man presented with rapidly progressive dementia (Figure 3). Angiography showed multiple DAVFs involving the superior sagittal sinus and the confluence of the sinuses. The bilateral transverse sinuses and superior sagittal sinus distal to the fistula were occluded and retrograde venous drainage was prominent. Bilateral external carotid branches were extensively embolized using PVA particles and NBCA. Angiography after transarterial embolization demonstrated persistent filling of the
fistulas, although the shunted blood flow was significantly reduced. He underwent intraoperative direct sinus packing. A postoperative angiography showed complete obliteration of both lesions, and the neurological symptoms also completely resolved. CASE 4 This 40-year-old man presented with papilledema and increased intracranial pressure (Figure 4). Angiography showed a DAVF of the superior sagittal sinus with leptomeningeal retrograde venous drainage and venous congestion of the bilateral cerebral hemispheres. The diseased sinus did not contribute to the venous drainage of the surrounding normal brain. First, a transfemoral venous approach to the diseased sinus was attempted but failed because of severe stenosis of the superior sagittal sinus proximal to the AVF. A cortical vein, draining the normal
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Case 2: left external carotid angiogram, arterial (A) and venous phase (B), and left occipital angiogram, lateral projection (C), showing a dural arteriovenous fistula (DAVF) at the origin of the vein of Labbe. Both retrograde and antegrade venous drainage were noted. (D) Postoperative left common carotid angiogram, lateral projection, showing complete disappearance of the DAVF. (E) Right internal carotid angiogram, venous phase, anteroposterior projection, showing the preserved left transeverse sinus.
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brain, went into the superior sagittal sinus just posterior to the AVF and it appeared difficult to occlude the AVF selectively, preserving this important cortical vein, under the guidance of intraoperative DSA. He underwent surgical excision. However, it was difficult to localize the lesion precisely and to differentiate the cortical veins with retrograde filling of the shunted blood flow from those draining the normal surrounding brain, and a postoperative angiogram showed small residual fistulas with retrograde venous drainage. However, the venous return from both cerebral hemispheres improved and symptoms of increased intracranial pressure were significantly reduced.
Results ANATOMIC RESULTS In 16 patients, postoperative angiography revealed complete disappearance of the DAVF. In one patient who underwent direct sinus packing for a DAVF of
the transverse sinus, intraoperative DSA after the packing was completed demonstrated persistent filling of the fistula draining into the vein of Labbe. Therefore, interruption of the vein of Labbe was performed, and postoperative angiography revealed no residual filling of the fistula. In 1 patient who underwent surgical excision of the diseased segment of the sinus, small residual fistulas were demonstrated on postoperative angiography (Figure 4). CLINICAL RESULTS Fourteen patients were clinically asymptomatic at final follow-up. The other 3 patients—2 presenting with aphasia caused by intracerebral hemorrhage and 1 presenting with consciousness disturbance (semicoma) caused by diffuse brain swelling— experienced significant clinical improvements after the treatment; however, mild aphasia and memory disturbances, respectively, remained. There were no treatment-related complications.
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Case 3: left external carotid angiogram, anteroposterior projection (A), lateral projection arterial phase (B), and venous phase (C), showing multiple DAVFs involving the superior sagittal sinus and the confluence of the sinuses. Bilateral transverse sinuses and superior sagittal sinus distal to the fistula were occluded and retrograde venous drainage was prominent. (D) Left external carotid angiogram, lateral projection, after the transarterial embolization showing significant reduction of the shunted blood flow. (E) Skull X-ray film after direct sinus packing, lateral projection, showing the coils in the affected sinuses. (F) Postoperative left common carotid angiogram, lateral projection, showing complete obliteration of both DAVFs.
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Discussion In patients with intracranial DAVFs, the most important factor that determines the clinical presentation and prognosis is restrictive change of venous out-
flow and venous drainage pattern [2,3,5,7,14]. To predict the clinical presentation and to guide therapeutic decision-making, several classifications of DAVFs have been developed considering these factors [2,5,14]. When the fistulas are drained only
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Case 4: left external carotid angiogram, anteroposterior projection (A) and lateral projection (B), showing a DAVF involving the superior sagittal sinus with leptomeningeal retrograde venous drainage. (C) Left external carotid angiogram, arterial phase oblique projection, showing the precise location of the DAVF (arrowheads). (D) Internal carotid angiogram, venous phase oblique projection, showing that the diseased sinus did not contribute to the venous drainage of the surrounding the normal brain and normal cortical vein went into the superior sagittal sinus just posterior to the DAVF. Arrow and curved arrow indicate the direction of the venous blood flow. (E) Postoperative right common carotid angiogram, lateral projection, showing a small residual DAVF with retrogade venous drainage (small arrows).
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through the sinus antegradely, they are usually asymptomatic and exhibit benign courses. In this type of DAVF, aggressive treatment such as transvenous embolization or surgical resection is not indicated because of the risks of venous infarction caused by occluding the venous drainage from normal brain tissue. On the other hand, when the fistulas have retro-
grade leptomeningeal venous drainage, they are associated with aggressive clinical behavior and require aggressive treatment. The goal of treatment is complete occlusion or at least conversion of a highrisk type to a low-risk type by eliminating the retrograde leptomeningeal drainage. Usually, in DAVFs with retrograde leptomeningeal venous drainage, these veins do not contribute to the venous drain-
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age from the normal brain tissue any more, and occlusion of the venous side of the fistula can be performed without risk of venous infarction. Therefore, percutaneous transvenous embolization is widely accepted as the first choice of treatment because of the lower invasiveness and high cure rate [11,16,19]. However, severe stenosis or bifocal occlusion of the venous outlet are not uncommon findings in these high-risk DAVFs, and make the percutaneous transvenous approach to the fistula difficult. In these situations, surgical interventions are required. Recent reports of histopathological examinations of DAVFs suggest that the essential lesion was direct communication between dural arteries and dural veins within the dural sinus wall, not a direct fistula between the arteries and the dural sinus [12,15]. The venous outflow may drain into the adjacent sinus or cortical veins. Surgical strategies should be chosen considering the angioarchitecture, especially the direction of venous drainage from the fistula. We simply classified the DAVFs into the following two subtypes based on the angiographical findings: (1) DAVFs with cortical venous drainage alone; (2) AVFs involving the dural sinus with leptomeningeal retrograde venous drainage. DAVFS WITH CORTICAL VENOUS DRAINAGE ALONE The angioarchitecture of this DAVF type is relatively simple, and surgical treatment is technically easy and safe [6,13,18]. When the venous drainage goes into the cortical vein retrogradely and there is no antegrade venous outflow into the neighboring sinus, complete and permanent obliteration can be achieved by simple interruption of the draining vein as close to the fistula as possible without excision of the AVF. This procedure can be performed via a small craniotomy and with minimal invasion of the brain. The present study included 8 patients with DAVFs with cortical venous drainage alone. In 1 patient, there was a large varix at the fistulous point and antegrade flow from this varix toward the sinus was also noted. Therefore, complete excision of the varix was performed in this patient. The other 7 patients underwent simple interruption of the draining vein and complete obliteration of the DAVF was achieved without any complications in all patients. When antegrade venous outflow into the sinus is also noted, it is important to differentiate this subgroup of DAVFs from those involving the dural sinus with retrograde leptomeningeal venous drainage. In Case 2, there was a large varix at the fistulous point, and antegrade flow from this varix
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toward the transverse sinus was also noted. Therefore, complete excision of the varix, preserving the patency of the transverse sinus, was performed in this patient. If it is misdiagnosed as a DAVF involving the sinus and occlusion or resection of the sinus is performed, it may result in worsening of the venous hypertension. When there is an arterial pedicle through which the microcatheter can be navigated close to the fistula, transarterial embolization with NBCA may provide complete obliteration of the lesion by penetrating distally to the proximal portion of the draining vein [1,5]. Because this is less invasive, transarterial embolization with NBCA may be used as the first choice of treatment, although the cure rate is not high. When the main arterial pedicles originate from the internal carotid or vertebral artery, or when the risk of occlusion of nutrient vessels of cranial nerves is high, transarterial embolization using NBCA should not be undertaken. Recent advancements in microcatheters and coils enable percutaneous transvenous embolization in this DAVF type in some specific cases [4, 8]. However, navigation of the microcatheter via the tortuous cortical vein is extremely hazardous and it should not be performed as the first choice of treatment. AVFS INVOLVING THE DURAL SINUS WITH RETROGRADE LEPTOMENINGEAL VENOUS DRAINAGE Usually, there are multiple small arterial pedicles and complete obliteration of the fistula by transarterial embolization alone is difficult [11,19]. The value of transarterial embolization preceding the curative treatment is controversial. It is suggested that particulate embolization is safe and effective to reduce the shunted blood flow and to facilitate subsequent transvenous embolization or surgery [6,10]. Moreover, superselective angiography may provide important information about the precise location of the lesion. The previously reported surgical procedure was as follows [6,17]: the affected dural sinus was exposed widely, the dura was incised on each side of the sinus until it was isolated completely, all the efferent arterialized veins were cut, and the sinus was ligated proximally and distally and removed. This is a more tedious procedure that may result in intradural complications and tremendous blood loss [17]. We performed surgical excision of the DAVF in only one patient with a superior sagittal sinus lesion (Figure 4). In this patient, it was difficult to localize the lesion precisely and to differentiate
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the cortical veins with retrograde filling of the shunted blood flow from those draining the normal surrounding brain. Therefore, the extent of the excision was insufficient and postoperative DSA revealed minimal persistent filling of the fistula. Transvenous embolization plays a key role in the curative treatment of AVFs involving the dural sinus [11,16,19]. When transfemoral venous access is difficult because of severe stenosis or bifocal occlusion of the sinus, intraoperative direct sinus packing is technically easy and effective, and is considered the first choice of treatment [9 –11,19]. Complete cure is not always achieved by transvenous embolization or direct sinus packing [10,11, 19], and some studies have emphasized the superiority of the surgical excision because of its high cure rate [6]. However, it is suggested that when intra- or postoperative control angiography reveals persistent filling of the fistula after the packing is completed, a complementary surgical excision or interruption of the draining vein should be performed [10]. This procedure can be performed more easily and safely after significant reduction of shunted blood flow by sinus packing compared with direct surgical excision without sinus packing. Endo et al suggest that a small craniotomy or burr hole is enough for direct sinus packing [9]. We prefer to expose the affected sinus widely. There is a possible subtype of DAVF involving both the dural sinus and cortical veins and it is sometimes difficult to differentiate this type from DAVFs involving only the dural sinus by preoperative examinations. In this subtype, occlusion of the sinus alone may result in persistent filling of the AVF with cortical venous drainage alone. In this situation, subsequent surgical procedures to occlude this remnant can be performed more easily through the wide operative field.
Conclusion 1. For high-risk DAVFs with leptomeningeal retrograde venous drainage, when embolization is technically difficult or has resulted in incomplete occlusion, surgical treatment is indicated. 2. When considering surgical strategies, it is essential to evaluate the precise location of the AVF, the anatomic features, and venous drainage from both the AVF and normal brain. 3. DAVFs with cortical venous drainage alone without dural sinus involvement are best treated by interruption of the draining vein close to the fistula. 4. AVFs involving the dural sinus with retrograde
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leptomeningeal venous drainage can be treated by transarterial embolization combined with direct tight packing of the diseased sinus for a high rate of cure and a low rate of morbidity. REFERENCES 1. Barnwell SL, Halbach VV, Dowd CF, Higashida RT, Hieshima GB, Wilson CB. A variant of arteriovenous fistulas within the wall of dural sinuses. Results of combined surgical and endovascular therapy. J Neurosurg 1991;74:199 –204. 2. Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 1995;82:166 –79. 3. Brown RD, Wiebers DO, Nichols DA. Intracranial dural arteriovenous fistulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 1994;81:531– 8. 4. Cloft HJ, Kallmes DF, Jensen ME, Dion JE. Percutaneous transvenous coil embolization of a Type 4 sagittal sinus dural arteriovenous fistula: case report. Neurosurgery 1997;41:1191– 4. 5. Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, Chiras J, Merland JJ. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 1995;194:671– 80. 6. Collice M, D’Aliberti G, Arena O, Solaini C, Fontana RA, Talamonti G. Surgical treatment of intracranial dural arteriovenous fistulae: role of venous drainage. Neurosurgery 2000;47:56 – 67. 7. Davies MA, TerBrugge K, Willinsky R, Coyne T, Saleh J, Wallace C. The Validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 1996;85:830 –7. 8. Defreyne L, Valangenhove P, Vandekerckhove T, Deschrijver I, Sieben G, Klaes R, Kunnen M. Transvenous embolization of a dural arteriovenous fistula of the anterior cranial fossa: Preliminary results. Am J Neuroradiol 2000;21:761–5. 9. Endo S, Kuwayama N, Takaku A, Nishijima M. Direct packing of the isolated sinus in patients with dural arteriovenous fistulas of the transverse-sigmoid sinus. J Neurosurg 1998;88:449 –56. 10. Goto K, Sidipratomo P, Ogata N, Inoue T, Matsuno H. Combining endovascular and neurosurgical treatments of high-risk dural arteriovenous fistulas in the lateral sinus and the confluence of the sinuses. J Neurosurg 1999;90:289 –99. 11. Halbach VV, Higashida RT, Hieshima GB, Mehringer CM, Hardin CW. Transvenous embolization of dural fistulas involving the transverse and sigmoid sinuses. Am J Neuroradiol 1989;10:385–92. 12. Hamada Y, Goto K, Inoue T, Iwaki T, Matsuno H, Suzuki S, Matsushima T, Fukui M, Miyake E. Histopathological aspects of dural arteriovenous fistulas in the transverse-sigmoid sinus region in nine patients. Neurosurgery 1997;40:452– 8. 13. Hoh BL, Choudhri TF, Connolly Jr ES, Solomon RA. Surgical management of high-grade intracranial dural arteriovenous fistulas: leptomeningeal venous disruption without nidus excision. Neurosurgery 1998; 42:796 – 805.
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14. Lalwani AK, Dowd CF, Halbach VV. Grading venous restrictive disease in patients with dural arteriovenous fistulas of the transverse/sigmoid sinus. J Neurosurg 1993;79:11–5. 15. Nishijima M, Takaku A, Endo S, Kuwayama N, Koizumi F, Sato H, Owada K. Etiological evaluation of dural arteriovenous malformations of the lateral and sigmoid sinuses based on histopathological examinations. J Neurosurg 1992;76:600 – 6. 16. Roy D, Raymond J. The role of transvenous embolization in the treatment of intracranial dural arteriovenous fistulas. Neurosurgery 1997;40:1133– 44. 17. Sundt TM, Piepgras DG. The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 1983;59:32–9. 18. Thompson BG, Doppman JL, Oldfield EH. Treatment of cranial dural arteriovenous fistulae by interruption of leptomeningeal venous drainage. J Neurosurg 1994; 80:617–23. 19. Urtasun F, Biondi A, Casasco A, Houdart E, Caputo N, Aymard A, Merland JJ. Cerebral dural arteriovenous fistulas: percutaneous transvenous embolization. Radiology 1996;199:209 –17.
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COMMENTARY
Ushikoshi and co-authors have collected a series of cases of dural fistulas associated with cortical venous drainage. There is no doubt that this is a subgroup of dural fistulas that puts the patient at risk of intraparenchymal hemorrhage or infarctions. Therefore, these patients must be treated aggressively. The authors have succeeded in curing this difficult-to-treat condition with a combination of embolization and surgical exposure. At surgery, they either resected the sinus, packed it with coils, or ligated the arterialized vein at the fistula level. They should be congratulated on their results. The progress in the development and navigation of microcatheters will continue to increase the number of these cases that can be cured with embolization alone. Gerard Debrun, M.D. Interventional Neuroradiologist Paris, France
hen I stand before God at the end of my life, I would hope that I would not have a single bit of talent left, and could say “I used everything you gave me.”
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—Erma Bombeck
n every outthrust headland, in every curving beach, in every grain of sand there is the story of the earth.
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—Rachel Carson