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Embolization of dural arteriovenous fistula of the anterior cranial fossa through the middle meningeal artery with Onyx
Clinical Neurology and Neurosurgery 117 (2014) 1–5
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Embolization of dural arteriovenous fistula of the anterior cranial fossa through the middle meningeal artery with Onyx Jian-Ping Deng, Jiang Li, Tao Zhang, Jia Yu, Zhen-Wei Zhao ∗,1 , Guo-Dong Gao 1 Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province 710038, China
a r t i c l e
i n f o
Article history: Received 25 May 2013 Received in revised form 12 August 2013 Accepted 16 November 2013 Available online 24 November 2013 Keywords: Dural arteriovenous fistula Embolization Onyx Anterior cranial fossa
a b s t r a c t Objective: Dural arteriovenous fistula (DAVF) of the anterior cranial fossa is usually treated by surgical disconnection or endovascular embolization via the ophthalmic artery. The middle meningeal artery is a rarely used approach. This study investigated the safety and efficacy of embolization of DAVF of the anterior cranial fossa with Onyx through the middle meningeal artery. Methods: A retrospective review of a prospective cerebral vascular disease database was performed. Patients with DAVF of the anterior cranial fossa managed with embolization through the middle meningeal artery with Onyx were selected. Information on demography, symptoms and signs, angiographic examinations, interventional treatments, angiographic and clinical results, and follow-up was collected and analyzed. Results: Five patients were included in this study, four of whom had hemorrhage. All fistulas were fed by the bilateral ethmoidal arteries arising from the ophthalmic artery and by the anterior branch of the middle meningeal artery. The abnormal shunt unilaterally drained into the superior sagittal sinus with interposition of the cortical veins all five patients. All endovascular treatments were successful with evidence of an angiographic cure. No complications occurred, and all patients recovered uneventfully without neurologic deficits. There were nearly no symptoms among the patients during follow-up. Conclusion: Embolization of DAVF of the anterior cranial fossa via the middle meningeal artery with Onyx is safe, effective, and a good choice for management of DAVF. More cases are needed to verify these findings. © 2013 Published by Elsevier B.V.
1. Introduction Dural arteriovenous fistula (DAVF) of the anterior cranial fossa is a rare lesion, accounting for only 5.8% of all cerebral DAVF [1–3]. This entity is divided into a special subgroup characterized by its high risk of hemorrhage, which occurs at a rate of 62–91% [2–8]. The modality of treatment for most cases in the literature is open surgery, which is safe and effective [1,4–7,9–13]. Endovascular embolization has been less frequently carried out because of the risk of eyesight damage or incomplete fistula occlusion [7–9,14–21]. Usually, access to the fistula is obtained through the ophthalmic artery with N-butyl cyanoacrylate and Onyx [7,8,14–18] or through a venous approach with coils [19–21]. The middle meningeal artery (MMA), which is usually the best choice for embolization of DAVF of other locations, is rarely selected. Only one case involving embolization with Onyx through the anterior branch of the MMA has been reported [16]. The present
∗ Corresponding author at: No. 1, Xinsi Road, Baqiao District, Xi’an City, Shaanxi Province 710038, China. Tel.: +86 29 84777285; fax: +86 29 84777435. E-mail address: [email protected] (Z.-W. Zhao). 1 These authors equally contributed to this study. 0303-8467/$ – see front matter © 2013 Published by Elsevier B.V. http://dx.doi.org/10.1016/j.clineuro.2013.11.013
case series aims to prove that an approach through the MMA with the use of Onyx is safe and effective. 2. Materials and methods A retrospective review of a prospective database on cerebral vascular disease was performed. All patients with DAVF of the anterior cranial fossa were included. The inclusion criterion was having undergone an approach to transarterial embolization through the MMA with Onyx. The exclusion criteria were having undergone other types of surgical management or embolization via other approaches. Information on patients’ demography, symptoms and signs, radiologic images, characteristics of digital subtraction angiography (DSA), process of interventional treatment, angiographic and clinical results, and follow-up was collected and analyzed. Diagnostic DSA of six arteries was performed for every patient before endovascular treatments. After induction of general anesthesia, a 6-F sheath was placed at the right femoral artery, and a 6-F guiding catheter (Envoy; Johnson & Johnson, Miami, FL, USA) was introduced into the ipsilateral external carotid artery (ECA). A microcatheter (Marathon; ev3 Neurovascular Inc., Irvine, CA, USA) was used to wedge the anterior branch of the MMA as close as possible to the fistula. Once the catheterization was done, the guiding
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catheter was retreated to the common carotid artery (CCA) when a branch of the internal carotid artery fed the fistula. If it was fed bilaterally, an angiographic catheter was placed at the contralateral CCA through another femoral approach for verification of embolization. Onyx (ev3 Neurovascular Inc., Irvine, CA, USA) was then injected through the microcatheter after flushing of DMSO (ev3 Neurovascular Inc., Irvine, CA, USA). Although the risk was small, attention was paid to prevent unexpected flow into the retinal artery. When the abnormal shunt had completely disappeared, the injection was stopped and all catheters were removed. Follow-up mainly involved symptoms and signs. Angiographic follow-up was supposed to for patient at about half and year. 3. Results A total of 26 patients were identified in the database. From January 2010 to December 2012, five patients treated with embolization via the MMA were selected. Two were female and three were male. Their age ranged from 38 to 71 years with an average of 56.8 years. Four patients presented with sudden headache; computed tomography (CT) showed hemorrhage located in the frontal lobe in one, a small subdural hematoma in two, and subarachnoid hemorrhage in one. The fifth patient complained of a slow-onset headache, and magnetic resonance imaging showed a vascular lesion lying on the anterior cranial fossa. Physical examination revealed no neurological abnormalities. 3.1. Angiographic images All fistulas were fed by the bilateral ethmoidal arteries arising from the ophthalmic artery. The bilateral ECAs were feeders for
four fistulas, and a unilateral ECA was a feeder for one fistula. The anterior branches of the MMA were unilaterally present in all five cases. In all five cases, the abnormal shunt was unilateral and drained directly into the cortical veins and then into the superior sagittal sinus. Venous dilatation of the aneurysmal pouch was present in four of the five cases. 3.2. Treatment All procedures were successfully performed. Both CCA angiograms immediately after injection showed total obliteration of the abnormal shunt. The duration of treatment from introduction of the guiding catheter to removal of the microcatheter was within 1 h in every case. An angiographic cure was achieved in all patients, and there were no complications. The four patients with hemorrhagic presentations recovered uneventfully and left the hospital with no neurological symptoms or signs. The fifth patient’s vision improved immediately after the embolization because of interruption of stolen blood flow, and the headache slowly disappeared. During a follow-up of 7–18 months, no new symptoms developed in any patient, and no follow-up angiography was performed. 3.3. Illustrative cases 3.3.1. Case 1 An elderly man suffered from headache. Magnetic resonance imaging revealed a vascular lesion in the anterior cranial fossa, and diagnostic DSA showed DAVF of the anterior cranial fossa fed by the ethmoidal branches of both ophthalmic arteries and dural branches of the left ECA, including the MMA (Fig. 1A and B). Interventional treatment was carried out. The Marathon microcatheter
Fig. 1. Lateral angiogram shows the fistula fed by (A) the left ophthalmic artery and (B) anterior branch of left middle meningeal artery. (C) The microcatheter reaches the fistula as confirmed by a microcatheter angiogram. (D and E) The abnormal shunt cannot be seen after injection. (F) The cast of Onyx is present at the fistula, showing the shape of the proximal ectatic drainage.
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reached the fistula through the anterior branch of the MMA (Fig. 1C). Onyx (0.8 mL) was injected and dispersed throughout the vascular networks close to the fistula (Fig. 1F). The abnormal shunt completely disappeared (Fig. 1D and E). Interestingly, the patient experienced great improvement in his eyesight immediately after treatment. A decline in eyesight due to the stolen blood supply was not realized before the procedure. 3.3.2. Case 2 A patient experienced a sudden headache, and CT revealed subarachnoid hemorrhage. DSA was performed because of suspicion of cerebral aneurysm. A DAVF in the anterior cranial fossa was found. The feeders included both ophthalmic arteries and the right ECA. The anterior branch of the right MMA was smooth and straight, and the aneurysmal pouch was clearly seen (Fig. 2A and B). The microcatheter easily arrived at the optimal site through the anterior branch of the MMA, which was confirmed on a microcatheter angiogram (Fig. 2C). The fistula was totally obliterated after injection of 1.2 mL of Onyx (Fig. 2D–F). The patient was discharged from the hospital with no neurologic deficits. 3.3.3. Case 3 A patient experienced a sudden headache, and CT revealed a small hematoma inside the frontal lobe. DSA showed a DAVF of the anterior cranial fossa fed by both ophthalmic arteries (Fig. 3A). Interestingly, the MMA fed the fistula at a different location (Fig. 3B). The microcatheter reached the fistula at the convexity of the frontal lobe (Fig. 3C). Although Onyx was only present inside the venous network on the convexity of the frontal lobe (Fig. 3D and E), the fistula was totally obliterated (Fig. 3F and G). The patient’s recovery was uneventful.
3
4. Discussion This was a small case series, and only five patients were included in this study. However, to our knowledge, it is the largest series of embolization management through the MMA. One other patient reported in the literature was treated with this technique [16]. The present five cases, though one was atypical in that it involved multiple fistulas at the convexity of the frontal lobe, clearly demonstrate the characteristics of DAVF of the anterior cranial fossa. All fistulas drained directly into the leptomeningeal vein with hypertrophic development of a varix, aneurysmal pouch, or tortuous pathway; in addition, bleeding was the first symptom in 80% of patients, similar to previous reports [2,3]. Therefore, aggressive treatment was necessary in this series. Embolization through the anterior branch of the MMA with Onyx was successful in this series of patients. The microcatheter easily reached the fistula, and Onyx injection was smoothly performed. All patients achieved an angiographic cure with no complications and recovered uneventfully. This series shows that embolization of DAVF of the anterior cranial fossa with Onyx via the MMA as a feeder is safe and effective. A review of our database indicated that nearly half of affected patients could be managed with this technique and were treated with surgical interruption in the past. Although access to the fistula may be difficult in cases involving an extremely tortuous MMA, this technique is a good treatment choice for many patients with DAVF of the anterior cranial fossa, as shown in this study. More cases are needed to confirm these findings. Traditionally, surgical interruption was the main choice to treat DAVF of the anterior cranial fossa with good safety and efficacy [1,4–7,9–13]. Endovascular embolization was seldom adopted. From 1990 to 2012, only 41 cases were managed endovascularly [7–9,14–21]. Most embolizations were carried out through the ophthalmic arteries [7,8,14–20], and few were carried out through
Fig. 2. Lateral angiogram shows the fistula fed by (A) the right ophthalmic artery and (B) a straight anterior branch of the right middle meningeal artery. (C) Catheterization was easily and successfully performed. (D–F) The fistula was resolved after injection of Onyx.
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Fig. 3. Lateral angiogram shows the fistula fed by (A) the right ophthalmic artery and (B) a straight anterior branch of the right middle meningeal artery. (C) Catheterization was easily and successfully performed. (D–F) The fistula was resolved after injection of Onyx.
the emissary artery [9] or by a venous approach [19–21]. Why was endovascular embolization infrequently used to treat DAVF of the anterior cranial fossa? First, catheterization through the tortuous ophthalmic artery is difficult. Thus, Li et al. required the assistance of a balloon [8]. Even if the catheter reached the optimal site, there was limited space for reflux because of potential injury to the central retinal artery. Sometimes the effect was sacrificed to avoid complications, which led to incomplete embolization. Agid reported 11 patients treated via the ophthalmic artery with N-butyl cyanoacrylate, four of whom underwent partial embolization [7]. The total rate of partial embolization in the literature is more than 10% (5/41), and a second treatment in such cases is inevitable. Second, a transvenous approach through the superior sagittal sinus is more difficult because of the tortuous draining vein and long distance. Only five cases have reportedly been managed with transvenous embolization [19–21]. Third, the importance of the anterior branch of the MMA as a good approach for embolization has not been adequately recognized. It is known that the posterior branch of the MMA is a very effective approach for embolization of DAVF located in the tentorium and transverse-sigmoid sinus area with Onyx [22–24]. Even if these branches are tiny or tortuous, a good surgical outcome is obtained. This technique has several advantages, such as less risky catheterization, strong resistance to rupture when pulling back the microcatheter, and enough space for reflux, which increases the strength of forward penetration of Onyx into the vascular networks including nearby drainage veins or feeders. The anterior branch of the MMA also has these characteristics. Why it has not been more frequently selected as an embolization approach is unclear; it is possible that most doctors believe that craniotomy should be performed in patients
with this lesion. Only one case of embolization through the anterior branch of the MMA with Onyx has been reported, and total obliteration and absence of complications were achieved in this case [16]. We expect that this small case series will help to give rise to endovascular management of DAVF of the anterior cranial fossa via the MMA with the herein-described approach. Although only five such cases were recently managed in our center, we found that half of the fistulas could be embolized with this technique. Compared with surgical interruption, it is less invasive and more cost-effective. It should be the first treatment choice for DAVF of the anterior cranial fossa if the MMA exists as a feeder, followed by surgical interruption. This is currently the strategy of choice in our center. Craniotomy is the first choice for fistulas without an MMA feeder. Although efforts were made to perform embolization via other approaches, such as through the septal artery of the internal maxillary artery with balloon assistance or balloon-assisted embolization through the ophthalmic artery, these approaches are difficult and complicated and cannot be used as regular modalities. Very complex manipulation would place the patient in a more dangerous situation.
5. Conclusion In this small case series of patients with DAVF of the anterior cranial fossa managed by embolization through an anterior branch of the MMA with Onyx, affected patients achieved an angiographic cure with no complications. These results show that this modality is safe and effective. On some occasions, it could be a very good
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treatment choice, even superior to surgical interruption. More cases are needed to verify these findings. Conflict of interest All authors were employed by one hospital. There is no potential conflict of interest. References [1] Halbach VV, Higashida RT, Hieshima GB, Wilson CB, Barnwell SL, Dowd CF. Dural arteriovenous fistulas supplied by ethmoidal arteries. Neurosurgery 1990;26:816–23. [2] Awad IA, Little JR, Akarawi WP, Ahl J. Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 1990;72:839–50. [3] Lasjaunias P, Chiu M, ter Bragge K, Tolia A, Hurth M, Bernstein M. Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 1986;64:724–30. [4] Tanei T, Fukui K, Wakabarashi K, Mitsui Y, Inoue N, Watanabe M. Dural arteriovenous fistula in the anterior cranial fossa: four case reports. Neurol Med Chir (Tokyo) 2008;48:560–3. [5] Hashiguchi A, Mimata C, Ichimura H, Morioka M, Kuratsu J. Venous aneurysm development associated with a dural arteriovenous fistula of the anterior cranial fossa with devastating hemorrhage. Neurol Med Chir (Tokyo) 2007;47:70–3. [6] Choi HJ, Cho CW. Anterior cranial fossa dural arteriovenous fistulae presenting as subdural hematoma. J Korean Neurosurg Soc 2010;47:155–7. [7] Agid R, Terbrugge K, Rodesch G, Andersson T, Soderman M. Management strategies for anterior cranial fossa (ethmoidal) dural arteriovenous fistulas with an emphasis on endovascular treatment. J Neurosurg 2009;110:79–84. [8] Li Q, Fang YB, Huang QH, Zhang Q, Hong B, Zhao WY, Liu JM, Xu Y. Transarterial embolization of dural arteriovenous fistulas of the anterior cranial fossa with Onyx. J Clin Neurosci 2013;20:287–91. [9] Lawton MT, Chun J, Wilson CB, Halbach VV. Ethmoidal dural arteriovenous fistulae: an assessment of surgical and endovascular management. Neurosurgery 1999;45:805–10. [10] Im SH, Oh CW, Han DH. Surgical management of an unruptured dural arteriovenous fistula of the anterior cranial fossa: natural history for 7 years. Surg Neurol 2004;62:72–5.
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[11] Mayfrank L, Reul J, Huffmann B, Bertalanffy H, Spetzger U, Gilsbach JM. Microsurgical interhemispheric approach to dural arteriovenous fistulas of the floor of the anterior cranial fossa. Minim Invasive Neurosurg 1996;39: 74–7. [12] 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;42:796–804. [13] Ros de San Pedro J, Pérez CJ, Parra JZ, Lopez-Guerrero AL, Sanchez JF. Bilateral ethmoidal dural arteriovenous fistula: unexpected surgical diagnosis. Clin Neurol Neurosurg 2010;112:903–8. [14] Guedin P, Gaillard S, Boulin A, Condette-Auliac S, Bourdain F, Guieu S, Dupuy M, Rodesch G. Therapeutic management of intracranial dural arteriovenous shunts with leptomeningeal venous drainage: report of 53 consecutive patients with emphasis on transarterial embolization with acrylic glues. J Neurosurg 2010;112:603–10. [15] Katsaridis V, Papagiannaki C, Visolaris C. Endovascular treatment of a bilateral ophthalmic-ethmoidal artery dural arteriovenous fistula. J Neuroophthalmol 2007;27:281–4. [16] Tahon F, Salkine F, Amsalem Y, Aguettaz P, Lamy B, Turjman F. Dural arteriovenous fistula of the anterior treated with the Onyx liquid embolic system and the Sonic microcatheter. Neuroradiology 2008;50:429–32. [17] Mack WJ, Gonzalez NR, Janhan R, Vinuela F. Endovascular management of anterior cranial fossa dural arteriovenous malformations: a technical report and anatomical discussion. Interv Neuroradiol 2011;17:93–103. [18] Lv XL, Li Y, Wu Z. Endovascular treatment of anterior cranial fossa dural arteriovenous fistula. Neuroradiology 2008;50:433–7. [19] Cognard C, Januel AC, Silva Jr NA, Tall P. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. AJNR Am J Neuroradiol 2008;29:235–41. [20] Kirsch M, Henkes K. A ruptured intraorbital ophthalmic artery aneurysm, associated with a dural arteriovenous fistula: combined transarterial and transvenous endovascular treatment. Minim Invasive Neurosurg 2011;54: 128–31. [21] Defreyne L, Vanlangenhove P, Vandekerckhove T, Deschrijver I, Klaes R, Kunnen M. Transvenous embolization of a dural arteriovenous fistula of the anterior cranial fossa: preliminary results. AJNR Am J Neuroradiol 2000;21:761–5. [22] Jiang C, Lv X, Li Y, Wu Z. Transarterial Onyx packing of the transverse-sigmoid sinus for dural arteriovenous fistulas. Eur J Radiol 2011;80:767–70. [23] Huang QH, Xu Y, Hong B, Li Q, Zhao W, Liu J. Use of Onyx in the management of tentorial dural arteriovenous fistulae. Neurosurgery 2009;65:287–93. [24] Nogueira RG, Dabus G, Rabinov JD, Rabinov JD, Eskey CJ, Ogilvy CS, Hirsch JA, Pryor JC. Preliminary experience with Onyx embolizaiton for the treatment of intracranial dural arteriovenous fistulas. AJNR Am J Neuroradiol 2008;29:91–7.
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Embolization of dural arteriovenous fistula of the anterior cranial fossa through the middle meningeal artery with Onyx Jian-Ping Deng, Jiang Li, Tao Zhang, Jia Yu, Zhen-Wei Zhao ∗,1 , Guo-Dong Gao 1 Department of Neurosurgery, Tangdu Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province 710038, China
a r t i c l e
i n f o
Article history: Received 25 May 2013 Received in revised form 12 August 2013 Accepted 16 November 2013 Available online 24 November 2013 Keywords: Dural arteriovenous fistula Embolization Onyx Anterior cranial fossa
a b s t r a c t Objective: Dural arteriovenous fistula (DAVF) of the anterior cranial fossa is usually treated by surgical disconnection or endovascular embolization via the ophthalmic artery. The middle meningeal artery is a rarely used approach. This study investigated the safety and efficacy of embolization of DAVF of the anterior cranial fossa with Onyx through the middle meningeal artery. Methods: A retrospective review of a prospective cerebral vascular disease database was performed. Patients with DAVF of the anterior cranial fossa managed with embolization through the middle meningeal artery with Onyx were selected. Information on demography, symptoms and signs, angiographic examinations, interventional treatments, angiographic and clinical results, and follow-up was collected and analyzed. Results: Five patients were included in this study, four of whom had hemorrhage. All fistulas were fed by the bilateral ethmoidal arteries arising from the ophthalmic artery and by the anterior branch of the middle meningeal artery. The abnormal shunt unilaterally drained into the superior sagittal sinus with interposition of the cortical veins all five patients. All endovascular treatments were successful with evidence of an angiographic cure. No complications occurred, and all patients recovered uneventfully without neurologic deficits. There were nearly no symptoms among the patients during follow-up. Conclusion: Embolization of DAVF of the anterior cranial fossa via the middle meningeal artery with Onyx is safe, effective, and a good choice for management of DAVF. More cases are needed to verify these findings. © 2013 Published by Elsevier B.V.
1. Introduction Dural arteriovenous fistula (DAVF) of the anterior cranial fossa is a rare lesion, accounting for only 5.8% of all cerebral DAVF [1–3]. This entity is divided into a special subgroup characterized by its high risk of hemorrhage, which occurs at a rate of 62–91% [2–8]. The modality of treatment for most cases in the literature is open surgery, which is safe and effective [1,4–7,9–13]. Endovascular embolization has been less frequently carried out because of the risk of eyesight damage or incomplete fistula occlusion [7–9,14–21]. Usually, access to the fistula is obtained through the ophthalmic artery with N-butyl cyanoacrylate and Onyx [7,8,14–18] or through a venous approach with coils [19–21]. The middle meningeal artery (MMA), which is usually the best choice for embolization of DAVF of other locations, is rarely selected. Only one case involving embolization with Onyx through the anterior branch of the MMA has been reported [16]. The present
∗ Corresponding author at: No. 1, Xinsi Road, Baqiao District, Xi’an City, Shaanxi Province 710038, China. Tel.: +86 29 84777285; fax: +86 29 84777435. E-mail address: [email protected] (Z.-W. Zhao). 1 These authors equally contributed to this study. 0303-8467/$ – see front matter © 2013 Published by Elsevier B.V. http://dx.doi.org/10.1016/j.clineuro.2013.11.013
case series aims to prove that an approach through the MMA with the use of Onyx is safe and effective. 2. Materials and methods A retrospective review of a prospective database on cerebral vascular disease was performed. All patients with DAVF of the anterior cranial fossa were included. The inclusion criterion was having undergone an approach to transarterial embolization through the MMA with Onyx. The exclusion criteria were having undergone other types of surgical management or embolization via other approaches. Information on patients’ demography, symptoms and signs, radiologic images, characteristics of digital subtraction angiography (DSA), process of interventional treatment, angiographic and clinical results, and follow-up was collected and analyzed. Diagnostic DSA of six arteries was performed for every patient before endovascular treatments. After induction of general anesthesia, a 6-F sheath was placed at the right femoral artery, and a 6-F guiding catheter (Envoy; Johnson & Johnson, Miami, FL, USA) was introduced into the ipsilateral external carotid artery (ECA). A microcatheter (Marathon; ev3 Neurovascular Inc., Irvine, CA, USA) was used to wedge the anterior branch of the MMA as close as possible to the fistula. Once the catheterization was done, the guiding
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catheter was retreated to the common carotid artery (CCA) when a branch of the internal carotid artery fed the fistula. If it was fed bilaterally, an angiographic catheter was placed at the contralateral CCA through another femoral approach for verification of embolization. Onyx (ev3 Neurovascular Inc., Irvine, CA, USA) was then injected through the microcatheter after flushing of DMSO (ev3 Neurovascular Inc., Irvine, CA, USA). Although the risk was small, attention was paid to prevent unexpected flow into the retinal artery. When the abnormal shunt had completely disappeared, the injection was stopped and all catheters were removed. Follow-up mainly involved symptoms and signs. Angiographic follow-up was supposed to for patient at about half and year. 3. Results A total of 26 patients were identified in the database. From January 2010 to December 2012, five patients treated with embolization via the MMA were selected. Two were female and three were male. Their age ranged from 38 to 71 years with an average of 56.8 years. Four patients presented with sudden headache; computed tomography (CT) showed hemorrhage located in the frontal lobe in one, a small subdural hematoma in two, and subarachnoid hemorrhage in one. The fifth patient complained of a slow-onset headache, and magnetic resonance imaging showed a vascular lesion lying on the anterior cranial fossa. Physical examination revealed no neurological abnormalities. 3.1. Angiographic images All fistulas were fed by the bilateral ethmoidal arteries arising from the ophthalmic artery. The bilateral ECAs were feeders for
four fistulas, and a unilateral ECA was a feeder for one fistula. The anterior branches of the MMA were unilaterally present in all five cases. In all five cases, the abnormal shunt was unilateral and drained directly into the cortical veins and then into the superior sagittal sinus. Venous dilatation of the aneurysmal pouch was present in four of the five cases. 3.2. Treatment All procedures were successfully performed. Both CCA angiograms immediately after injection showed total obliteration of the abnormal shunt. The duration of treatment from introduction of the guiding catheter to removal of the microcatheter was within 1 h in every case. An angiographic cure was achieved in all patients, and there were no complications. The four patients with hemorrhagic presentations recovered uneventfully and left the hospital with no neurological symptoms or signs. The fifth patient’s vision improved immediately after the embolization because of interruption of stolen blood flow, and the headache slowly disappeared. During a follow-up of 7–18 months, no new symptoms developed in any patient, and no follow-up angiography was performed. 3.3. Illustrative cases 3.3.1. Case 1 An elderly man suffered from headache. Magnetic resonance imaging revealed a vascular lesion in the anterior cranial fossa, and diagnostic DSA showed DAVF of the anterior cranial fossa fed by the ethmoidal branches of both ophthalmic arteries and dural branches of the left ECA, including the MMA (Fig. 1A and B). Interventional treatment was carried out. The Marathon microcatheter
Fig. 1. Lateral angiogram shows the fistula fed by (A) the left ophthalmic artery and (B) anterior branch of left middle meningeal artery. (C) The microcatheter reaches the fistula as confirmed by a microcatheter angiogram. (D and E) The abnormal shunt cannot be seen after injection. (F) The cast of Onyx is present at the fistula, showing the shape of the proximal ectatic drainage.
J.-P. Deng et al. / Clinical Neurology and Neurosurgery 117 (2014) 1–5
reached the fistula through the anterior branch of the MMA (Fig. 1C). Onyx (0.8 mL) was injected and dispersed throughout the vascular networks close to the fistula (Fig. 1F). The abnormal shunt completely disappeared (Fig. 1D and E). Interestingly, the patient experienced great improvement in his eyesight immediately after treatment. A decline in eyesight due to the stolen blood supply was not realized before the procedure. 3.3.2. Case 2 A patient experienced a sudden headache, and CT revealed subarachnoid hemorrhage. DSA was performed because of suspicion of cerebral aneurysm. A DAVF in the anterior cranial fossa was found. The feeders included both ophthalmic arteries and the right ECA. The anterior branch of the right MMA was smooth and straight, and the aneurysmal pouch was clearly seen (Fig. 2A and B). The microcatheter easily arrived at the optimal site through the anterior branch of the MMA, which was confirmed on a microcatheter angiogram (Fig. 2C). The fistula was totally obliterated after injection of 1.2 mL of Onyx (Fig. 2D–F). The patient was discharged from the hospital with no neurologic deficits. 3.3.3. Case 3 A patient experienced a sudden headache, and CT revealed a small hematoma inside the frontal lobe. DSA showed a DAVF of the anterior cranial fossa fed by both ophthalmic arteries (Fig. 3A). Interestingly, the MMA fed the fistula at a different location (Fig. 3B). The microcatheter reached the fistula at the convexity of the frontal lobe (Fig. 3C). Although Onyx was only present inside the venous network on the convexity of the frontal lobe (Fig. 3D and E), the fistula was totally obliterated (Fig. 3F and G). The patient’s recovery was uneventful.
3
4. Discussion This was a small case series, and only five patients were included in this study. However, to our knowledge, it is the largest series of embolization management through the MMA. One other patient reported in the literature was treated with this technique [16]. The present five cases, though one was atypical in that it involved multiple fistulas at the convexity of the frontal lobe, clearly demonstrate the characteristics of DAVF of the anterior cranial fossa. All fistulas drained directly into the leptomeningeal vein with hypertrophic development of a varix, aneurysmal pouch, or tortuous pathway; in addition, bleeding was the first symptom in 80% of patients, similar to previous reports [2,3]. Therefore, aggressive treatment was necessary in this series. Embolization through the anterior branch of the MMA with Onyx was successful in this series of patients. The microcatheter easily reached the fistula, and Onyx injection was smoothly performed. All patients achieved an angiographic cure with no complications and recovered uneventfully. This series shows that embolization of DAVF of the anterior cranial fossa with Onyx via the MMA as a feeder is safe and effective. A review of our database indicated that nearly half of affected patients could be managed with this technique and were treated with surgical interruption in the past. Although access to the fistula may be difficult in cases involving an extremely tortuous MMA, this technique is a good treatment choice for many patients with DAVF of the anterior cranial fossa, as shown in this study. More cases are needed to confirm these findings. Traditionally, surgical interruption was the main choice to treat DAVF of the anterior cranial fossa with good safety and efficacy [1,4–7,9–13]. Endovascular embolization was seldom adopted. From 1990 to 2012, only 41 cases were managed endovascularly [7–9,14–21]. Most embolizations were carried out through the ophthalmic arteries [7,8,14–20], and few were carried out through
Fig. 2. Lateral angiogram shows the fistula fed by (A) the right ophthalmic artery and (B) a straight anterior branch of the right middle meningeal artery. (C) Catheterization was easily and successfully performed. (D–F) The fistula was resolved after injection of Onyx.
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Fig. 3. Lateral angiogram shows the fistula fed by (A) the right ophthalmic artery and (B) a straight anterior branch of the right middle meningeal artery. (C) Catheterization was easily and successfully performed. (D–F) The fistula was resolved after injection of Onyx.
the emissary artery [9] or by a venous approach [19–21]. Why was endovascular embolization infrequently used to treat DAVF of the anterior cranial fossa? First, catheterization through the tortuous ophthalmic artery is difficult. Thus, Li et al. required the assistance of a balloon [8]. Even if the catheter reached the optimal site, there was limited space for reflux because of potential injury to the central retinal artery. Sometimes the effect was sacrificed to avoid complications, which led to incomplete embolization. Agid reported 11 patients treated via the ophthalmic artery with N-butyl cyanoacrylate, four of whom underwent partial embolization [7]. The total rate of partial embolization in the literature is more than 10% (5/41), and a second treatment in such cases is inevitable. Second, a transvenous approach through the superior sagittal sinus is more difficult because of the tortuous draining vein and long distance. Only five cases have reportedly been managed with transvenous embolization [19–21]. Third, the importance of the anterior branch of the MMA as a good approach for embolization has not been adequately recognized. It is known that the posterior branch of the MMA is a very effective approach for embolization of DAVF located in the tentorium and transverse-sigmoid sinus area with Onyx [22–24]. Even if these branches are tiny or tortuous, a good surgical outcome is obtained. This technique has several advantages, such as less risky catheterization, strong resistance to rupture when pulling back the microcatheter, and enough space for reflux, which increases the strength of forward penetration of Onyx into the vascular networks including nearby drainage veins or feeders. The anterior branch of the MMA also has these characteristics. Why it has not been more frequently selected as an embolization approach is unclear; it is possible that most doctors believe that craniotomy should be performed in patients
with this lesion. Only one case of embolization through the anterior branch of the MMA with Onyx has been reported, and total obliteration and absence of complications were achieved in this case [16]. We expect that this small case series will help to give rise to endovascular management of DAVF of the anterior cranial fossa via the MMA with the herein-described approach. Although only five such cases were recently managed in our center, we found that half of the fistulas could be embolized with this technique. Compared with surgical interruption, it is less invasive and more cost-effective. It should be the first treatment choice for DAVF of the anterior cranial fossa if the MMA exists as a feeder, followed by surgical interruption. This is currently the strategy of choice in our center. Craniotomy is the first choice for fistulas without an MMA feeder. Although efforts were made to perform embolization via other approaches, such as through the septal artery of the internal maxillary artery with balloon assistance or balloon-assisted embolization through the ophthalmic artery, these approaches are difficult and complicated and cannot be used as regular modalities. Very complex manipulation would place the patient in a more dangerous situation.
5. Conclusion In this small case series of patients with DAVF of the anterior cranial fossa managed by embolization through an anterior branch of the MMA with Onyx, affected patients achieved an angiographic cure with no complications. These results show that this modality is safe and effective. On some occasions, it could be a very good
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