The Neuroradiology Journal 21: 406-414, 2008
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Transarterial Embolization of Tentorial Dural Arteriovenous Fistulas with Onyx 18 XIANLI LV, CHUHAN JIANG, YOUXIANG LI, XINJIAN YANG, ZHONGXUE WU Beijing Neurosurgical institute, Beijing, the People’s Republic of China Beijing Tiantan Hospital, Capital Medical University, Beijing, the People’s Republic of China
Key words: intracranial, arteriovenous malformation, embolization
SUMMARY – Dural arteriovenous fistulas (DVAFs) have been reported to be treated transarterially with Onyx 18. We present a series of tentorial DAVFs treated by transarterial embolization with Onyx 18 over an 18-month period. Eight patients with tentorial DAVFs were treated between September 2005 and February 2007. All patients were treated transarterially with Onyx 18. The clinical presentation, treatment strategies and results were studied. Eight patients presented with intracranial hemorrhage or progressive neurological deficits. Retrograde leptomeningeal venous drainage was documented in every patient, classifying the lesions as Cognard Type IV. Post treatment angiography demonstrated complete obliteration in six cases. Clinical follow up ranged from six to 14 months. One patient experienced neurological decline after endovascular treatment and exhibited clinical improvement. There were no episodes of rehemorrhage or new neurological deficits. Outcomes were excellent in seven patients, fair in one case. Transarterial embolization of tentorial DAVF is feasible and may result in complete occlusion of the fistulous connection with liquid nonadhesives. Introduction The treatment strategy for tentorial DAVFs is still debated because of the rich variety of their flow types and the surgical difficulty for such deeply seated lesions 5,9,12,13,15. Dural arteriovenous fistulas (DVAFs) involving the superior sagittal sinus and the lesser sphenoid wing region have been treated transarterially with Onyx 18 1,17. Although transarterial embolization alone for tentorial DAVFs is rarely successful 2,5,10,11,15, we present a series of tentorial DAVFs well treated by transarterial embolization with Onyx 18. Patients and Methods Eight patients with symptomatic tentorial DAVFs were evaluated and treated at Beijing Tiantan Hospital between September 2005 and February 2007. All patients underwent six-vessel cerebral angiographic evaluations before treatment. Lesions were graded according to the classification system developed by Cognard et Al 4. 406
Endovascular Therapy The recently used transarterial approach involved the initial placement of a guiding catheter into the external carotid artery via a transfemoral approach. DAVF feeders were superselectively catheterized with a microcatheter (Marathon; MTI-EV3, Irvine, CA, USA) over a microwire (Mirage, MTI-EV3, Irvine, CA, USA). To treat the lesions, Onyx 18 (MTIEV3, Irvine, CA, USA) was used as the embolic agent in an attempt to “push” the glue across the arteriovenous shunts and into the proximal draining vein. In the meantime, a checking catheter was placed in the ipsilateral internal carotid artery or vertebral artery if necessary. Post treatment evaluation Patient outcomes were clinically graded at the first follow-up evaluation after discharge from the hospital. Clinical outcomes were graded with the Glasgow Outcome Scale (GOS). Excellent outcomes were defined as the resumption of normal life despite minor deficits (GOS=5). Good outcomes were defined as moderate disabilities with independence (GOS=4). Fair out-
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Transarterial Embolization of Tentorial Dural Arteriovenous Fistulas with Onyx 18
comes were defined as severe disabilities with dependence on the care of others (GOS=3). Poor outcomes were defined as persistent vegetative states (GOS=2) or death (GOS=1). Results Eight patients with Cognard Grade IV tentorial DAVFs were evaluated in this series. There were six male and two female patients, with ages ranging from 23 to 60 years (mean age, 46.3 yrs). Hemorrhage was present in six patients (6/8). One presented with right hemihypoesthesia, left occulomotor palsy, left hemifacial numbness and left tinnitus due to mass effect of dilated leptomeningeal veins. Another presented with headaches and intracranial bruits. Table 1 presents a complete profile of patients in this series.
Complications Trigeminocardiac reflex During Onyx injection, a reproducible bradycardia occurred in patient 6 (1/8). The explanation for this phenomenon was trigeminocardiac reflex (TCR). TCR has been described in the literature as a reflexive response of bradycardia, hypotension and gastric hypermobility seen upon mechanical stimulation in the distribution of the trigeminal nerve. Cranial Nerve Deficits after Embolization Hemifacial numbness and hemifacial palsy occurred after the procedure in patient 6 (1/8). The etiology was probably the embolization of the petrosal branch from the middle meningeal artery. The damage to the V and VII cranial nerves was transient and the patients showed complete recovery.
Angiographic Analysis
Posterior Fossa Infarction
All lesions were Cognard Type IV. The arterial supply was predominantly from the external carotid artery and always involved the middle meningeal artery. The few contributions from the internal carotid artery were via the meningohypophyseal trunk. The presence of a tentorial DAVF with retrograde leptomeningeal venous drainage was angiographically documented for all eight patients.
One patient with a tentorial DAVF fed by branches of the right external carotid artery and the left superior cerebellar artery developed brain infarction after the second procedure. After the second procedure, complete obliteration was achieved with catheterization of the superior cerebellar artery. The patient exhibited vertigo, diplopia, blepharoptosis, gustatory loss and deterioration of ataxia after the procedure. Post-procedure day 3, MRI examination (not shown) demonstrated infarctions of the left cerebellar hemisphere, the left side of the mesencephalic tegmentum and the left middle cerebellar peduncle.
Embolization All the patients were treated with transarterial embolization. Single injections of Onyx were carried out for up to 80 minutes with good arteriovenous shunt penetration. During injections, we were able to pause, obtain an angiogram to evaluate arteriovenous shunt occlusion and the status of the venous drainage, and then continue the injection with the same catheter. These maneuvers allowed for controlled delivery of the embolic agent. Arteriovenous shunt penetration was particularly good when the catheter achieved a wedged position in the feeding vessel. No venous occlusions occurred in our patients. When no venous migration was found, the injection was stopped to allow for solidification, then the injection was continued. The Onyx then filled a different portion of the lesion. The most amount of Onyx injected in one patient (Patient 7) was 9 ml. Six patients (6/8) experienced complete radiological cures.
Gluing of the Catheter A single instance of gluing catheter to the vessel occurred due to long reflux and single injection up to 25 minutes. The microcatheter was left in the body and an antiplatelet agent (aspirin) was administered after procedure. The patient remained asymptomatic. Clinical Outcome The clinical follow-up periods averaged 9.7 months approximately, with a range of six to 14 months. Seven patients in this series were without any neurological deficits while one patient showed diplopia, blepharoptosis, gustatory loss and mild ataxia. The patient with hemifacial numbness and hemifacial palsy 407
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Table1 Patient clinical courses and outcomes Patient Age/Sex No. 1
23/M
2.
55/F
3.
41/F
4.
60/M
Cognard Type
Presentation Intracerebellar hemorrhage Intracerebellar hemorrhage Intracerebellar hemorrhage Intracerebellar hemorrhage
IV IV IV IV
5.
48/M
Hemihypoesthesia (R) CN (III, V) deficits (L), Tinnitus (L)
6.
42/M
Intracerebellar hemorrhage
7.
49/M
8.
52/M
Intracerebellar, hemorrhage Headaches, intracranial bruits
Venous drainage
Suppliers MMA (L), MHT (L)
BVR, varix
MMA (R), MHT (R) OA (R), PMA (R) MMA (L), MHT (L) OA (L) MMA (B), MHT, OA APA, SCA
Treatment strategy
Amount of Onyx 18
Duration time
TAE
2.5 ml
25 min
VOG, varix TAE
2.7 ml
not recorded
BVR,varix
TAE
4.5 ml
40 min
BVR, dilated
TAE(I)
5.0 ml
50 min
TAE(II)
0.7 ml
not recorded
MMA (L), MHT (B) OA (L), IMA (L), AMA (L)
BVR, varix
TAE
3.5 ml
50 min
MMA (R), MHT (R) SCA (R)
Cerebellar veins, PV, varix
TAE
2.5 ml
80 min
IV
MMA (L), MHT (L)
PV, varix
TAE
9.0 ml
not recorded
IV
MMA (L), IMA (L)
SPS, varix
TAE
4.0 ml
not recorded
IV
BVR, basal vein of Rosenthal; CN, cranial nerve; ICH, intracranial hemorrhage; IMA, internal maxillary artery branches; MMA, middle meningeal artery branches; MHT, meningohypophyseal trunk branches; OA, occipital artery; PMA, posterior meningeal artery; APA, ascending pharyngeal artery; SCA, superior cerebellar artery; TAE, transarterial embolization; VOG, vein of Galen; PV, petrosal vein
Patient No.
Angiographic results
1.
Complete
2.
Complications
Follow-up
Clinical outcome
Gluing of microcatheter
7.5 months
GOS=5, no symptoms
Incomplete
None
6.0 months
GOS=5, no symptoms
3.
Complete
None
14. months
GOS=5, no symptoms
4.
Incomplete (I) Complete (II)
5.
Complete
6.
Incomplete
7. 8.
None vertigo, diplopia, blepharoptosis, taxia, hemihypoesthesia, gustatory loss
12. months
GOS=5, no symptoms GOS=4, diplopia,blepharoptosis hemihypoesthesia,gustatory loss mild ataxial.
None
12. months
GOS=5, no symptoms
Trigemino-cardiac reflex, hemifacial numbness, hemifacial palsy
8.0 months
GOS=5, no symptoms, hemifacial numbness, resolved within 2 months; hemifacial palsy, resolved within 3 months
Complete
None
12. months
GOS=5, no symptoms
Complete
None
6.0 months
GOS=5, no symptoms
I, the first stage; II, the second stage; GOS, Glasgow Outcome Scale.
showed recovery at post procedure two months and three months. There was no further deterioration. Illustrative Cases Patient 3 This 41-year-old woman presented with sudden headache and unconsciousness two months previously (figure 1). CT scanning revealed in408
tracerebellar hemorrhage at that time and the hemotoma was removed by surgery. The neurological examination in our institution showed ataxia and angiography revealed a DAVF involving the left cerebellar tentorium. The left middle meningeal artery was wedged and the DAVF was embolized using Onyx 18. Angiography after transarterial embolization showed complete obliteration of the lesion. After the procedure, the patient was discharged on the postembolization day 3 without any complication.
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The Neuroradiology Journal 21: 406-414, 2008
B
Figure 1 Patient 3: left external carotid angiogram, lateral projection arterial phase (A) showing a DAVF involving the left cerebellar tentorium. B) Left common carotid angiogram, anteroposterior projection after the transarterial embolization showing complete obliteration of the DAVF.
Patient 5
Discussion
A 48-year-old man presented with right hemihypoesthesia, left occulomotor palsy, left hemifacial numbness and left tinnitus (figure 2). Angiography revealed the DAVF directly emptying into the basal vein of Rosenthal. The left middle meningeal artery was catheterized as close to the DAVF as possible and embolization with Onyx was performed. Complete obliteration was achieved. At present, no abnomalities are seen in his neurological examination.
Tentorial DAVFs are located in the cerebellar tentorium and are fed primarily from branches of the meningohypophysial trunk, the middle meningeal artery and occipital artery. Although venous drainage varies greatly and depends on the tentorial location of the fistula, they typically drain into deep leptomeningeal veins 5,8-10. Thus, tentorial DAVFs are aggressive, 80%-90% presenting with hemorrhage 5,6,9-11,16 , as illustrated by our patients: six out of eight patients presented with intracerebellar hemorrhage and were shown to have venous aneurysms and retrograde filling of cortical veins. These lesions require prompt, complete treatment, as partial therapy is not fully protective 5. Tentorial DAVFs can be treated by transarterial or transvenous embolization 2,3,5,10,11,25 , stereotactic radiosurgery 8,12,13, surgical resection 6,8,9,11,14 or some combination of these strategies 7,11,21. Surgical division of the tentorial DAVF is extremely difficult because of the deep locations of the lesions, with surrounding vital structures such as the deep venous system 6,9,12. Complete interruption of a DAVF must be confirmed intraoperatively by visual inspection, intraoperative angiography and intraoperative microvascular Doppler monitoring 7. Although
Patient 7 A 49-year-old man presented with intracerebellar hemorrhage (figure 3). A cerebral angiogram demonstrated a DAVF of the tentorium, which was fed predominantly by the posterior branch of the left middle meningeal artery and the left meningohypophyseal trunk and drained to the transverse sinus via an ecstatic leptomeningeal vein. The left middle meningeal artery was catheterized with a Marathon microcatheter. Excellent penetration of the arteriovenous shunts was achieved after injecting 9 ml Onyx. After the embolization, the fistula was obliterated completely and the patient remains neurologically intact.
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A
B
C
D
several cases of tentorial DAVF have been treated by transvenous embolization 5, venous approach through the elongated, ectactic and potentially fragile pial veins is considered difficult and risky. Previously, embolization by a transarterial approach that used flow control via a single remaining feeder after occluding all other contributing pedicles seemed to be the best option 2,11. Treatment with gamma knife is also reported to be effective, but the risk of bleeding remains until a cure is obtained 8,12,13. Highly flexible, hydrophilic distal navigation 410
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permits complete occlusion of a dural arteriovenous shunt via endoarterial route only. This technique may be facilitated by a limited number of feeding vessels and a wedged position that allows injection of liquid embolic agent in a relatively controlled fashion. In our own recent experience, we were able to treat high grade DAVFs successfully by means of this technique. Its main drawback is that these lesions frequently have a complex arterial supply, which leads to difficulty in occluding the arteriovenous shunts. Catheterization of the
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Figure 2 Patient 5: left common carotid angiogram, lateral projection (A) and the left internal carotid angiogram, lateral projection (B) showing a dural arteriovenous fistula of the tentorium. C) Onyx was injected via the right middle meningeal artery. Left external carotid angiogram (D) and the left internal carotid angiogram, lateral projection (E), after the embolization showing complete obliteration of the fistula. F) Skull X-ray film after embolization, lateral projection, showing the cast of Onyx 18 in the left middle meningeal artery.
tentorial artery from the internal carotid artery was performed by van Rooij et Al to treat tentorial DAVFs 26. However, we usually selected the external carotid branches as the approaches to treat, because of their safety, and cure can be achieved even it is not the main feeding vessel. To prevent the inherent risk of reflux of glue into the internal carotid or vertebral artery, the patency of the internal carotid artery or vertebral artery was checked frequently during Onyx injection. Because revascularization will follow only if the arterial inflow is interrupted
, Onyx should be pushed until it reaches the initial venous drainage. Although intravascular embolization is the procedure of choice, few reports have indicated that embolization results in complete and permanent lesion obliteration 10 . In previous cases, 19 patients were treated by transarterial embolization but only three fistulas were completely occluded 10. However, in our series, arterial embolization was used as a sole therapy with the aim of cure. Success in our embolization is facilitated by the controllable liquid embolic agent.
9
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Transarterial Embolization of Tentorial Dural Arteriovenous Fistulas with Onyx 18
A
B
C
D
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Figure 3 Patient 7 Left external carotid angiogram (A) and left internal carotid angiogram (B) show a DAVF involving the tentorium fed by bilateral meningohypopheseal trunk and left external carotid artery (C) showing the posterior branch of the left middle meningeal artery was catheterized. After embolization, the left common carotid angiogram (D) shows the lesion was completely obliterated.
Platinum coils and NBCA have been used as embolic agents for treatment of DAVFs in our institute before. It is well known that the recanalization rate is lower with cyanoacrylate liquid adhesives. Compared with NBCA, Onyx is a nonadhesive liquid embolic agent, and does not polymerize but the EVOH copolymer precipitates while the DMSO diffuses under aqueous conditions, and thus mechanically occludes the 412
feeding vessels 20,22,24. The nonadhesive property of Onyx allows the surgeon far greater latitude in varying the rate of injection and the amount of the agent delivered during a single injection. In the external carotid territory, a longer reflux of Onyx around the tip of the microcatheter can be achieved more safely compared with the pial arteries, provided that the microcatheter is placed sufficiently distally. As long as the oper-
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ator is confident that he will be able to retrieve the microcatheter, this long reflux may create sufficient proximal flow arrests to enable better distal penetration 18,19. Consequently, when used in dural fistulas, it may be more realistic to consider Onyx as a potential permanent embolic agent, rather than expecting it to be surgically removed. In this study the largest amount of Onyx used was 9 ml and the patient was uneventful after injection so we believe the Onyx is safe for treatment. Three adverse events occurred in our series as outlined in detail above. Despite the nonadhesive property of Onyx, in one instance, a single injection up to 25 minutes, the microcatheter was glued to the vessel. We suggest that the duration of a single injection not exceed 25 minutes if there is a long reflex. The other two adverse events are directly related to the Onyx reflux. Trigeminocardiac Reflex This reproducible response occurred in patient 6 (1/8). The reflexic bradycardia seen during Onyx injection is not likely attributable to other factors. The whole procedure was performed under a standardized anesthetic protocol. We did not irritate the brain to produce the reflex. A study on anesthesia monitoring in patients treated with Onyx embolization for intracranial aneurysms showed that no changes in heart rate or blood pressure occurred following DMSO and Onyx injections, nor were any arrythmias observed 14. We consider that this response is one of TCR 23. TCR has been described in the literature as a reflexive response of bradycardia, hypotension, and gastric hypermobility seen upon mechanical stimulation in the distribution of the trigeminal nerve 1820 . Clinically, TCR has been reported to occur during tumor resection in the cerebellopontine angle 20 and falx cerebri 18, and transsphenoidal surgery for pituitary adenomas 18. TCR as a physiological reflex has been clarified 19. When stimulation causes TCR, treatment of hemodynamic instability consists of ceasing the proce-
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dure and anticholinergic drugs should be administered. Atropine was shown to extinguish the TCR effectively in our patients. Anticholinergic drugs are not given prophylactically because they can cause refractory arrhythmias 18,20. Cranial Nerve Deficits after Embolization We think that occlusion of the cavernous branch and petrosal branch occurring as Onyx refluxed into the pedicle of the middle meningeal artery may result in trigeminal and facial nerve deficits. This can be supported by fact that the patients complained of the hemifacial numbness and dull sensation to touch along the innervation of the second and third trigeminal divisions. Our patients recovered facial sensation within two months and facial function within three months after the procedure. Although this complication is reversible. Onyx injection should be paused while it begins to permeate into some small branches, which are invisible on angiography but are functional. We believe that the recovery of facial function and sensation was the result of the vascular insult to the facial nerve. In addition, the embolization procedure itself may have caused additional vascular insult to the nerve. In our series, a posterior fossa infarction occurred, so we do not recommend the brain artery to be an approach. Further follow-up data are needed to determine the exact role of Onyx in the treatment of dural arteriovenous fistulas. Conclusion Tentorial DAVFs are aggressive lesions that require prompt total angiographic obliteration. Disconnection of the venous drainage from the fistula may be accomplished with transarterial embolization to the venous side. We think that transarterial embolization with Onyx 18 is an alternative to NBCA and surgery in treating tentorial DAVFs.
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References 1 Anil A, Servet I: Treatment of a superior sagittal sinus dural arteriovenous fistula with Onyx: Technical case report. Neurosurgery 59: 169-170, 2006. 2 Benndorf G, Schmidt S, Sollman WP et Al: Tentorial dural arteriovenous fistula presenting with various visual symptoms related to anterior and posterior visual pathway dysfunction: case report. Neurosurgery 53: 222-227, 2003. 3 Brano G, Takahashi A, Ezura M et Al: Dural arteriovenous shunt involving the superior petrosal sinus: presentation and treatment by transvenous embolization via the occipital and transverse sinuses. Neuroradiology 39: 67-70, 1997. 4 Cognard C, Gobin YP, Pierot L et Al: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194: 671-680, 1995. 5 Deasy NP, Gholkar AR, Cox TCS et Al: Tentorial dural arteriovenous fistulae: endovascular treatment with transvenous coil embolization. Neuradiology 41: 308312, 1999. 6 Deshmukh VR, Maughan PH, Spetzler RF: Resolution of hemifacial spasm after surgical obliteration of a tentorial arteriovenous fistula: case report. Neurosurgery 58: 202, 2006. 7 Fujita A, Tamaki N, Nakamura M et Al: A tentorial dural arteriovenous fistula successfully treated with interruption of leptomeningeal venous drainage using microvascular Doppler sonography: case report. Surg Neurol 56: 56-61, 2001. 8 Iwamuro Y, Nakahara I, Higashi T et Al: Tentorial dural arteriovenous fistula presenting symptoms due to mass effect on the dilated draining vein: case report. Surg Neurol 65: 511-515, 2006. 9 Jesus OD, Rosado JE: Tentorial dural arteriovenous fistula obliteration using the petrosal approach. Surg Neurol 51: 164-167, 1999. 10 Kajita Y, Miyachi S, Wakabayashi T et Al: A dural arteriovenous fistula of the tentorium successfully treated by intravascular embolization. Surg Neurol 52: 294-298, 1999. 11 Kim MS, Han DH, Han MH et Al: Posterior fossa hemorrhage caused by dural arteriovenous fistula: case reports. Surg Neurol 59: 512-517, 2003. 12 Masahiro S, Hiroki K, Masao T et Al: Stereotactic radiosurgery for tentorial dural arteriovenous fistulae draining into the vein of Galen: reports of two cases. Neurosurgery 46: 730, 2000. 13 Matsushige T, Nakaoka M, Ohta K et Al: Tentorial dural arteriovenous malformation manifesting as trigeminal neuralgia treated by stereotactic radiosurgery: a case report. Surg Neurol 66: 519-523, 2006. 14 Pannu Y, Shownkeen H, Nockels RP et Al: Obliteration of a tentorial dural arteriovenous fistula causing spinal cord myelopathy using the cranio-orbital zygomatic approach. Surg Neurol 62: 463-467, 2004. 15 Patrik RT, Harry JC, Akihiko K et Al: Evolution of the management of tentorial dural arteriovenous malformations. Neurosurgery 52: 750-762, 2003. 16 Paula-Lucas C, Pereica-Caldas J-G-M, Prandini MN: Do lepto meningeal venous drainage and dysplastic venous dilation predict hemorrhage in dural arteriovenous fistula? Surg Neurol 66: 2-3:6, 2006. 17 Rezende MTS, Poitin M, Mounayer C et Al: Dural arteriovenous fistula of the lesser sphenoid wing region treated with Onyx: technical note. Neuroradiology 48: 130-134, 2006. 18 Schaller B: Trigemino-cardiac reflex during transsphenoidal surgery for pituitary adenomas. Clin Neurol Neurosurg 107: 468-474, 2005. 19 Schaller B: Trigeminocardiac reflex: A clinical phenomenon or a new physiological entity? J Neurol 251: 658665, 2004.
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20 Schaller B, Probster R, Strebal S et Al: Trigemino-cardiac reflex during surgery in the cerebellopontine angle. J Neurosurg 90: 215-220, 1999. 21 Troffkin NA, Graham CB, Berkman T et Al: Combined transvenous and transarterial embolization of a tentorial-incisural dural arteriovenous malformation followed by primary stent placement in the associated stenotic straight sinus. Case report. J. Neurosurg 99: 579-583, 2003. 22 Yuichi M, Fernando V, Alexandre U et Al: Nonadhesive liquid embolic agent for cerebral arteriovenous malformations: Preliminary histopathological studies in Swine Rete Mirabile. Neurosurgery 43: 1164-1172, 1998. 23 Lv X, Li Y, Lv M et Al: Trigeminocardiac reflex in embolization of intracranial dural arteriovenous fistula. AJNR Am J Neuroradiol 28: 1769-1770, 2007. 24 Lv X, Li Y, Liu A et Al: Transarterial Embolization of Dural Arteriovenous Fistulas of the Anterior Cranial Fossa Onyx-18: Case Report. Neuroradiol J 20: 53-59, 2007. 25 Jiang C, Lv X, Li Y et Al: Transarterial and transvenous embolization for tentorial dural arteriovenous fistula: case report. Neuroradiol J 20: 726-729, 2007. 26 van Rooij WJ, Sluzewski M, Beute GN: Tentorial artery embolization in tentorial dural arteriovenous fistulas. Neuroradiology 48:737-743,2006.
Chuhan Jiang, MD Beijing Neurosurgical Institute Beijing Tiantan Hospital Capital Medical University 6,Tiantan Xili Beijing, Heibei 100050 China Tel.: 86-10-67098850 E-mail: [email protected]
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Transarterial Embolization of Tentorial Dural Arteriovenous Fistulas with Onyx 18 XIANLI LV, CHUHAN JIANG, YOUXIANG LI, XINJIAN YANG, ZHONGXUE WU Beijing Neurosurgical institute, Beijing, the People’s Republic of China Beijing Tiantan Hospital, Capital Medical University, Beijing, the People’s Republic of China
Key words: intracranial, arteriovenous malformation, embolization
SUMMARY – Dural arteriovenous fistulas (DVAFs) have been reported to be treated transarterially with Onyx 18. We present a series of tentorial DAVFs treated by transarterial embolization with Onyx 18 over an 18-month period. Eight patients with tentorial DAVFs were treated between September 2005 and February 2007. All patients were treated transarterially with Onyx 18. The clinical presentation, treatment strategies and results were studied. Eight patients presented with intracranial hemorrhage or progressive neurological deficits. Retrograde leptomeningeal venous drainage was documented in every patient, classifying the lesions as Cognard Type IV. Post treatment angiography demonstrated complete obliteration in six cases. Clinical follow up ranged from six to 14 months. One patient experienced neurological decline after endovascular treatment and exhibited clinical improvement. There were no episodes of rehemorrhage or new neurological deficits. Outcomes were excellent in seven patients, fair in one case. Transarterial embolization of tentorial DAVF is feasible and may result in complete occlusion of the fistulous connection with liquid nonadhesives. Introduction The treatment strategy for tentorial DAVFs is still debated because of the rich variety of their flow types and the surgical difficulty for such deeply seated lesions 5,9,12,13,15. Dural arteriovenous fistulas (DVAFs) involving the superior sagittal sinus and the lesser sphenoid wing region have been treated transarterially with Onyx 18 1,17. Although transarterial embolization alone for tentorial DAVFs is rarely successful 2,5,10,11,15, we present a series of tentorial DAVFs well treated by transarterial embolization with Onyx 18. Patients and Methods Eight patients with symptomatic tentorial DAVFs were evaluated and treated at Beijing Tiantan Hospital between September 2005 and February 2007. All patients underwent six-vessel cerebral angiographic evaluations before treatment. Lesions were graded according to the classification system developed by Cognard et Al 4. 406
Endovascular Therapy The recently used transarterial approach involved the initial placement of a guiding catheter into the external carotid artery via a transfemoral approach. DAVF feeders were superselectively catheterized with a microcatheter (Marathon; MTI-EV3, Irvine, CA, USA) over a microwire (Mirage, MTI-EV3, Irvine, CA, USA). To treat the lesions, Onyx 18 (MTIEV3, Irvine, CA, USA) was used as the embolic agent in an attempt to “push” the glue across the arteriovenous shunts and into the proximal draining vein. In the meantime, a checking catheter was placed in the ipsilateral internal carotid artery or vertebral artery if necessary. Post treatment evaluation Patient outcomes were clinically graded at the first follow-up evaluation after discharge from the hospital. Clinical outcomes were graded with the Glasgow Outcome Scale (GOS). Excellent outcomes were defined as the resumption of normal life despite minor deficits (GOS=5). Good outcomes were defined as moderate disabilities with independence (GOS=4). Fair out-
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Transarterial Embolization of Tentorial Dural Arteriovenous Fistulas with Onyx 18
comes were defined as severe disabilities with dependence on the care of others (GOS=3). Poor outcomes were defined as persistent vegetative states (GOS=2) or death (GOS=1). Results Eight patients with Cognard Grade IV tentorial DAVFs were evaluated in this series. There were six male and two female patients, with ages ranging from 23 to 60 years (mean age, 46.3 yrs). Hemorrhage was present in six patients (6/8). One presented with right hemihypoesthesia, left occulomotor palsy, left hemifacial numbness and left tinnitus due to mass effect of dilated leptomeningeal veins. Another presented with headaches and intracranial bruits. Table 1 presents a complete profile of patients in this series.
Complications Trigeminocardiac reflex During Onyx injection, a reproducible bradycardia occurred in patient 6 (1/8). The explanation for this phenomenon was trigeminocardiac reflex (TCR). TCR has been described in the literature as a reflexive response of bradycardia, hypotension and gastric hypermobility seen upon mechanical stimulation in the distribution of the trigeminal nerve. Cranial Nerve Deficits after Embolization Hemifacial numbness and hemifacial palsy occurred after the procedure in patient 6 (1/8). The etiology was probably the embolization of the petrosal branch from the middle meningeal artery. The damage to the V and VII cranial nerves was transient and the patients showed complete recovery.
Angiographic Analysis
Posterior Fossa Infarction
All lesions were Cognard Type IV. The arterial supply was predominantly from the external carotid artery and always involved the middle meningeal artery. The few contributions from the internal carotid artery were via the meningohypophyseal trunk. The presence of a tentorial DAVF with retrograde leptomeningeal venous drainage was angiographically documented for all eight patients.
One patient with a tentorial DAVF fed by branches of the right external carotid artery and the left superior cerebellar artery developed brain infarction after the second procedure. After the second procedure, complete obliteration was achieved with catheterization of the superior cerebellar artery. The patient exhibited vertigo, diplopia, blepharoptosis, gustatory loss and deterioration of ataxia after the procedure. Post-procedure day 3, MRI examination (not shown) demonstrated infarctions of the left cerebellar hemisphere, the left side of the mesencephalic tegmentum and the left middle cerebellar peduncle.
Embolization All the patients were treated with transarterial embolization. Single injections of Onyx were carried out for up to 80 minutes with good arteriovenous shunt penetration. During injections, we were able to pause, obtain an angiogram to evaluate arteriovenous shunt occlusion and the status of the venous drainage, and then continue the injection with the same catheter. These maneuvers allowed for controlled delivery of the embolic agent. Arteriovenous shunt penetration was particularly good when the catheter achieved a wedged position in the feeding vessel. No venous occlusions occurred in our patients. When no venous migration was found, the injection was stopped to allow for solidification, then the injection was continued. The Onyx then filled a different portion of the lesion. The most amount of Onyx injected in one patient (Patient 7) was 9 ml. Six patients (6/8) experienced complete radiological cures.
Gluing of the Catheter A single instance of gluing catheter to the vessel occurred due to long reflux and single injection up to 25 minutes. The microcatheter was left in the body and an antiplatelet agent (aspirin) was administered after procedure. The patient remained asymptomatic. Clinical Outcome The clinical follow-up periods averaged 9.7 months approximately, with a range of six to 14 months. Seven patients in this series were without any neurological deficits while one patient showed diplopia, blepharoptosis, gustatory loss and mild ataxia. The patient with hemifacial numbness and hemifacial palsy 407
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Table1 Patient clinical courses and outcomes Patient Age/Sex No. 1
23/M
2.
55/F
3.
41/F
4.
60/M
Cognard Type
Presentation Intracerebellar hemorrhage Intracerebellar hemorrhage Intracerebellar hemorrhage Intracerebellar hemorrhage
IV IV IV IV
5.
48/M
Hemihypoesthesia (R) CN (III, V) deficits (L), Tinnitus (L)
6.
42/M
Intracerebellar hemorrhage
7.
49/M
8.
52/M
Intracerebellar, hemorrhage Headaches, intracranial bruits
Venous drainage
Suppliers MMA (L), MHT (L)
BVR, varix
MMA (R), MHT (R) OA (R), PMA (R) MMA (L), MHT (L) OA (L) MMA (B), MHT, OA APA, SCA
Treatment strategy
Amount of Onyx 18
Duration time
TAE
2.5 ml
25 min
VOG, varix TAE
2.7 ml
not recorded
BVR,varix
TAE
4.5 ml
40 min
BVR, dilated
TAE(I)
5.0 ml
50 min
TAE(II)
0.7 ml
not recorded
MMA (L), MHT (B) OA (L), IMA (L), AMA (L)
BVR, varix
TAE
3.5 ml
50 min
MMA (R), MHT (R) SCA (R)
Cerebellar veins, PV, varix
TAE
2.5 ml
80 min
IV
MMA (L), MHT (L)
PV, varix
TAE
9.0 ml
not recorded
IV
MMA (L), IMA (L)
SPS, varix
TAE
4.0 ml
not recorded
IV
BVR, basal vein of Rosenthal; CN, cranial nerve; ICH, intracranial hemorrhage; IMA, internal maxillary artery branches; MMA, middle meningeal artery branches; MHT, meningohypophyseal trunk branches; OA, occipital artery; PMA, posterior meningeal artery; APA, ascending pharyngeal artery; SCA, superior cerebellar artery; TAE, transarterial embolization; VOG, vein of Galen; PV, petrosal vein
Patient No.
Angiographic results
1.
Complete
2.
Complications
Follow-up
Clinical outcome
Gluing of microcatheter
7.5 months
GOS=5, no symptoms
Incomplete
None
6.0 months
GOS=5, no symptoms
3.
Complete
None
14. months
GOS=5, no symptoms
4.
Incomplete (I) Complete (II)
5.
Complete
6.
Incomplete
7. 8.
None vertigo, diplopia, blepharoptosis, taxia, hemihypoesthesia, gustatory loss
12. months
GOS=5, no symptoms GOS=4, diplopia,blepharoptosis hemihypoesthesia,gustatory loss mild ataxial.
None
12. months
GOS=5, no symptoms
Trigemino-cardiac reflex, hemifacial numbness, hemifacial palsy
8.0 months
GOS=5, no symptoms, hemifacial numbness, resolved within 2 months; hemifacial palsy, resolved within 3 months
Complete
None
12. months
GOS=5, no symptoms
Complete
None
6.0 months
GOS=5, no symptoms
I, the first stage; II, the second stage; GOS, Glasgow Outcome Scale.
showed recovery at post procedure two months and three months. There was no further deterioration. Illustrative Cases Patient 3 This 41-year-old woman presented with sudden headache and unconsciousness two months previously (figure 1). CT scanning revealed in408
tracerebellar hemorrhage at that time and the hemotoma was removed by surgery. The neurological examination in our institution showed ataxia and angiography revealed a DAVF involving the left cerebellar tentorium. The left middle meningeal artery was wedged and the DAVF was embolized using Onyx 18. Angiography after transarterial embolization showed complete obliteration of the lesion. After the procedure, the patient was discharged on the postembolization day 3 without any complication.
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B
Figure 1 Patient 3: left external carotid angiogram, lateral projection arterial phase (A) showing a DAVF involving the left cerebellar tentorium. B) Left common carotid angiogram, anteroposterior projection after the transarterial embolization showing complete obliteration of the DAVF.
Patient 5
Discussion
A 48-year-old man presented with right hemihypoesthesia, left occulomotor palsy, left hemifacial numbness and left tinnitus (figure 2). Angiography revealed the DAVF directly emptying into the basal vein of Rosenthal. The left middle meningeal artery was catheterized as close to the DAVF as possible and embolization with Onyx was performed. Complete obliteration was achieved. At present, no abnomalities are seen in his neurological examination.
Tentorial DAVFs are located in the cerebellar tentorium and are fed primarily from branches of the meningohypophysial trunk, the middle meningeal artery and occipital artery. Although venous drainage varies greatly and depends on the tentorial location of the fistula, they typically drain into deep leptomeningeal veins 5,8-10. Thus, tentorial DAVFs are aggressive, 80%-90% presenting with hemorrhage 5,6,9-11,16 , as illustrated by our patients: six out of eight patients presented with intracerebellar hemorrhage and were shown to have venous aneurysms and retrograde filling of cortical veins. These lesions require prompt, complete treatment, as partial therapy is not fully protective 5. Tentorial DAVFs can be treated by transarterial or transvenous embolization 2,3,5,10,11,25 , stereotactic radiosurgery 8,12,13, surgical resection 6,8,9,11,14 or some combination of these strategies 7,11,21. Surgical division of the tentorial DAVF is extremely difficult because of the deep locations of the lesions, with surrounding vital structures such as the deep venous system 6,9,12. Complete interruption of a DAVF must be confirmed intraoperatively by visual inspection, intraoperative angiography and intraoperative microvascular Doppler monitoring 7. Although
Patient 7 A 49-year-old man presented with intracerebellar hemorrhage (figure 3). A cerebral angiogram demonstrated a DAVF of the tentorium, which was fed predominantly by the posterior branch of the left middle meningeal artery and the left meningohypophyseal trunk and drained to the transverse sinus via an ecstatic leptomeningeal vein. The left middle meningeal artery was catheterized with a Marathon microcatheter. Excellent penetration of the arteriovenous shunts was achieved after injecting 9 ml Onyx. After the embolization, the fistula was obliterated completely and the patient remains neurologically intact.
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Transarterial Embolization of Tentorial Dural Arteriovenous Fistulas with Onyx 18
A
B
C
D
several cases of tentorial DAVF have been treated by transvenous embolization 5, venous approach through the elongated, ectactic and potentially fragile pial veins is considered difficult and risky. Previously, embolization by a transarterial approach that used flow control via a single remaining feeder after occluding all other contributing pedicles seemed to be the best option 2,11. Treatment with gamma knife is also reported to be effective, but the risk of bleeding remains until a cure is obtained 8,12,13. Highly flexible, hydrophilic distal navigation 410
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permits complete occlusion of a dural arteriovenous shunt via endoarterial route only. This technique may be facilitated by a limited number of feeding vessels and a wedged position that allows injection of liquid embolic agent in a relatively controlled fashion. In our own recent experience, we were able to treat high grade DAVFs successfully by means of this technique. Its main drawback is that these lesions frequently have a complex arterial supply, which leads to difficulty in occluding the arteriovenous shunts. Catheterization of the
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F
Figure 2 Patient 5: left common carotid angiogram, lateral projection (A) and the left internal carotid angiogram, lateral projection (B) showing a dural arteriovenous fistula of the tentorium. C) Onyx was injected via the right middle meningeal artery. Left external carotid angiogram (D) and the left internal carotid angiogram, lateral projection (E), after the embolization showing complete obliteration of the fistula. F) Skull X-ray film after embolization, lateral projection, showing the cast of Onyx 18 in the left middle meningeal artery.
tentorial artery from the internal carotid artery was performed by van Rooij et Al to treat tentorial DAVFs 26. However, we usually selected the external carotid branches as the approaches to treat, because of their safety, and cure can be achieved even it is not the main feeding vessel. To prevent the inherent risk of reflux of glue into the internal carotid or vertebral artery, the patency of the internal carotid artery or vertebral artery was checked frequently during Onyx injection. Because revascularization will follow only if the arterial inflow is interrupted
, Onyx should be pushed until it reaches the initial venous drainage. Although intravascular embolization is the procedure of choice, few reports have indicated that embolization results in complete and permanent lesion obliteration 10 . In previous cases, 19 patients were treated by transarterial embolization but only three fistulas were completely occluded 10. However, in our series, arterial embolization was used as a sole therapy with the aim of cure. Success in our embolization is facilitated by the controllable liquid embolic agent.
9
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Transarterial Embolization of Tentorial Dural Arteriovenous Fistulas with Onyx 18
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B
C
D
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Figure 3 Patient 7 Left external carotid angiogram (A) and left internal carotid angiogram (B) show a DAVF involving the tentorium fed by bilateral meningohypopheseal trunk and left external carotid artery (C) showing the posterior branch of the left middle meningeal artery was catheterized. After embolization, the left common carotid angiogram (D) shows the lesion was completely obliterated.
Platinum coils and NBCA have been used as embolic agents for treatment of DAVFs in our institute before. It is well known that the recanalization rate is lower with cyanoacrylate liquid adhesives. Compared with NBCA, Onyx is a nonadhesive liquid embolic agent, and does not polymerize but the EVOH copolymer precipitates while the DMSO diffuses under aqueous conditions, and thus mechanically occludes the 412
feeding vessels 20,22,24. The nonadhesive property of Onyx allows the surgeon far greater latitude in varying the rate of injection and the amount of the agent delivered during a single injection. In the external carotid territory, a longer reflux of Onyx around the tip of the microcatheter can be achieved more safely compared with the pial arteries, provided that the microcatheter is placed sufficiently distally. As long as the oper-
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ator is confident that he will be able to retrieve the microcatheter, this long reflux may create sufficient proximal flow arrests to enable better distal penetration 18,19. Consequently, when used in dural fistulas, it may be more realistic to consider Onyx as a potential permanent embolic agent, rather than expecting it to be surgically removed. In this study the largest amount of Onyx used was 9 ml and the patient was uneventful after injection so we believe the Onyx is safe for treatment. Three adverse events occurred in our series as outlined in detail above. Despite the nonadhesive property of Onyx, in one instance, a single injection up to 25 minutes, the microcatheter was glued to the vessel. We suggest that the duration of a single injection not exceed 25 minutes if there is a long reflex. The other two adverse events are directly related to the Onyx reflux. Trigeminocardiac Reflex This reproducible response occurred in patient 6 (1/8). The reflexic bradycardia seen during Onyx injection is not likely attributable to other factors. The whole procedure was performed under a standardized anesthetic protocol. We did not irritate the brain to produce the reflex. A study on anesthesia monitoring in patients treated with Onyx embolization for intracranial aneurysms showed that no changes in heart rate or blood pressure occurred following DMSO and Onyx injections, nor were any arrythmias observed 14. We consider that this response is one of TCR 23. TCR has been described in the literature as a reflexive response of bradycardia, hypotension, and gastric hypermobility seen upon mechanical stimulation in the distribution of the trigeminal nerve 1820 . Clinically, TCR has been reported to occur during tumor resection in the cerebellopontine angle 20 and falx cerebri 18, and transsphenoidal surgery for pituitary adenomas 18. TCR as a physiological reflex has been clarified 19. When stimulation causes TCR, treatment of hemodynamic instability consists of ceasing the proce-
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dure and anticholinergic drugs should be administered. Atropine was shown to extinguish the TCR effectively in our patients. Anticholinergic drugs are not given prophylactically because they can cause refractory arrhythmias 18,20. Cranial Nerve Deficits after Embolization We think that occlusion of the cavernous branch and petrosal branch occurring as Onyx refluxed into the pedicle of the middle meningeal artery may result in trigeminal and facial nerve deficits. This can be supported by fact that the patients complained of the hemifacial numbness and dull sensation to touch along the innervation of the second and third trigeminal divisions. Our patients recovered facial sensation within two months and facial function within three months after the procedure. Although this complication is reversible. Onyx injection should be paused while it begins to permeate into some small branches, which are invisible on angiography but are functional. We believe that the recovery of facial function and sensation was the result of the vascular insult to the facial nerve. In addition, the embolization procedure itself may have caused additional vascular insult to the nerve. In our series, a posterior fossa infarction occurred, so we do not recommend the brain artery to be an approach. Further follow-up data are needed to determine the exact role of Onyx in the treatment of dural arteriovenous fistulas. Conclusion Tentorial DAVFs are aggressive lesions that require prompt total angiographic obliteration. Disconnection of the venous drainage from the fistula may be accomplished with transarterial embolization to the venous side. We think that transarterial embolization with Onyx 18 is an alternative to NBCA and surgery in treating tentorial DAVFs.
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References 1 Anil A, Servet I: Treatment of a superior sagittal sinus dural arteriovenous fistula with Onyx: Technical case report. Neurosurgery 59: 169-170, 2006. 2 Benndorf G, Schmidt S, Sollman WP et Al: Tentorial dural arteriovenous fistula presenting with various visual symptoms related to anterior and posterior visual pathway dysfunction: case report. Neurosurgery 53: 222-227, 2003. 3 Brano G, Takahashi A, Ezura M et Al: Dural arteriovenous shunt involving the superior petrosal sinus: presentation and treatment by transvenous embolization via the occipital and transverse sinuses. Neuroradiology 39: 67-70, 1997. 4 Cognard C, Gobin YP, Pierot L et Al: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194: 671-680, 1995. 5 Deasy NP, Gholkar AR, Cox TCS et Al: Tentorial dural arteriovenous fistulae: endovascular treatment with transvenous coil embolization. Neuradiology 41: 308312, 1999. 6 Deshmukh VR, Maughan PH, Spetzler RF: Resolution of hemifacial spasm after surgical obliteration of a tentorial arteriovenous fistula: case report. Neurosurgery 58: 202, 2006. 7 Fujita A, Tamaki N, Nakamura M et Al: A tentorial dural arteriovenous fistula successfully treated with interruption of leptomeningeal venous drainage using microvascular Doppler sonography: case report. Surg Neurol 56: 56-61, 2001. 8 Iwamuro Y, Nakahara I, Higashi T et Al: Tentorial dural arteriovenous fistula presenting symptoms due to mass effect on the dilated draining vein: case report. Surg Neurol 65: 511-515, 2006. 9 Jesus OD, Rosado JE: Tentorial dural arteriovenous fistula obliteration using the petrosal approach. Surg Neurol 51: 164-167, 1999. 10 Kajita Y, Miyachi S, Wakabayashi T et Al: A dural arteriovenous fistula of the tentorium successfully treated by intravascular embolization. Surg Neurol 52: 294-298, 1999. 11 Kim MS, Han DH, Han MH et Al: Posterior fossa hemorrhage caused by dural arteriovenous fistula: case reports. Surg Neurol 59: 512-517, 2003. 12 Masahiro S, Hiroki K, Masao T et Al: Stereotactic radiosurgery for tentorial dural arteriovenous fistulae draining into the vein of Galen: reports of two cases. Neurosurgery 46: 730, 2000. 13 Matsushige T, Nakaoka M, Ohta K et Al: Tentorial dural arteriovenous malformation manifesting as trigeminal neuralgia treated by stereotactic radiosurgery: a case report. Surg Neurol 66: 519-523, 2006. 14 Pannu Y, Shownkeen H, Nockels RP et Al: Obliteration of a tentorial dural arteriovenous fistula causing spinal cord myelopathy using the cranio-orbital zygomatic approach. Surg Neurol 62: 463-467, 2004. 15 Patrik RT, Harry JC, Akihiko K et Al: Evolution of the management of tentorial dural arteriovenous malformations. Neurosurgery 52: 750-762, 2003. 16 Paula-Lucas C, Pereica-Caldas J-G-M, Prandini MN: Do lepto meningeal venous drainage and dysplastic venous dilation predict hemorrhage in dural arteriovenous fistula? Surg Neurol 66: 2-3:6, 2006. 17 Rezende MTS, Poitin M, Mounayer C et Al: Dural arteriovenous fistula of the lesser sphenoid wing region treated with Onyx: technical note. Neuroradiology 48: 130-134, 2006. 18 Schaller B: Trigemino-cardiac reflex during transsphenoidal surgery for pituitary adenomas. Clin Neurol Neurosurg 107: 468-474, 2005. 19 Schaller B: Trigeminocardiac reflex: A clinical phenomenon or a new physiological entity? J Neurol 251: 658665, 2004.
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20 Schaller B, Probster R, Strebal S et Al: Trigemino-cardiac reflex during surgery in the cerebellopontine angle. J Neurosurg 90: 215-220, 1999. 21 Troffkin NA, Graham CB, Berkman T et Al: Combined transvenous and transarterial embolization of a tentorial-incisural dural arteriovenous malformation followed by primary stent placement in the associated stenotic straight sinus. Case report. J. Neurosurg 99: 579-583, 2003. 22 Yuichi M, Fernando V, Alexandre U et Al: Nonadhesive liquid embolic agent for cerebral arteriovenous malformations: Preliminary histopathological studies in Swine Rete Mirabile. Neurosurgery 43: 1164-1172, 1998. 23 Lv X, Li Y, Lv M et Al: Trigeminocardiac reflex in embolization of intracranial dural arteriovenous fistula. AJNR Am J Neuroradiol 28: 1769-1770, 2007. 24 Lv X, Li Y, Liu A et Al: Transarterial Embolization of Dural Arteriovenous Fistulas of the Anterior Cranial Fossa Onyx-18: Case Report. Neuroradiol J 20: 53-59, 2007. 25 Jiang C, Lv X, Li Y et Al: Transarterial and transvenous embolization for tentorial dural arteriovenous fistula: case report. Neuroradiol J 20: 726-729, 2007. 26 van Rooij WJ, Sluzewski M, Beute GN: Tentorial artery embolization in tentorial dural arteriovenous fistulas. Neuroradiology 48:737-743,2006.
Chuhan Jiang, MD Beijing Neurosurgical Institute Beijing Tiantan Hospital Capital Medical University 6,Tiantan Xili Beijing, Heibei 100050 China Tel.: 86-10-67098850 E-mail: [email protected]
