Clinical approach of using Onyx via transarterial access in treating tentorial dural arteriovenous fistula Chuanghong Liu1, Bin Xu2, Donglei Song3, Bing Leng2, Ying Mao2, Yuxiang Gu2, Yujun Liao2 1
Department of Neurosurgery, Changshu First People Hospital, Suzhou University, P. R. China, 2Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, P. R. China, 3Department of Neurosurgery, Deji Hospital, Shanghai, P. R. China Objective: In this study, based on clinical presentation and angiographic findings, we try to investigate the possibility to do transarterial embolization using Onyx to treat tentorial dural arteriovenous fistula (TDAVF). Particular attention will be given to the relationship between vascular anatomic characteristics and clinical management. Methods: We retrospectively reviewed the clinical and radiologic data of 26 patients with TDAVFs, who were treated via transarterial approach using Onyx (including three cases treating with balloon assisting) at our department from January 2005 to April 2010. Results: The total obliterated rate was 85.7, 53.8, and 66.7% in the tentorial marginal, lateral, and medial subtype, respectively. Symptoms were improved significantly in the patients whose fistulas were totally and sub-totally obliterated. The mean follow-up duration was 2.9 years. After operation, patients’ symptom was dramatically improved indicated by the decrease of individual modified Rankin scale (MRS). Only one patient suffered from temporary paralysis of cranial nerve (CN) III. All 26 patients were clinically stable and without any relapsed, increased, or new symptoms. All patients had resumed their normal activities until the latest follow-up. Conclusion: Treating the TDAVF via transarterial approach using Onyx maybe a feasible clinical practice. The fistula obliterated rate is highly related to the anatomic characteristic, and high complete obliterated rate can be achieved. Our preliminary results showed that Onyx injection with ‘balloon assisting’ technique can be helpful in some of the cases.
Keywords: Tentorial, Dural arteriovenous fistula, Onyx
Abbreviations
Background
TDAVF, tentorial dural arteriovenous fistula; ECA external carotid artery; M male; F female; SAH subarachnoid hemorrhage; CN cranial nerve; SPA sphenopalatine artery; MHT meningohypophyseal trunk branches; MMA middle meningeal artery; OA occipital artery; PMA posterior meningeal artery; PCA posterior cerebral artery; TCT truncus costocervicalis; BVR basal vein of Rosenthal; VOG vein of Galen; ICA internal carotid artery; CT computed tomography; MRI magnetic resonance imaging; DSA digital subtraction angiography; MRS modified Rankin scale.
Tentorial dural arteriovenous fistula (TDAVF) is a relatively rare lesion, accounting for 4–8.4% of all the intracranial DAVFs.1,2 However, 97% of the patients have hemorrhage or progressive focal neurological deficits because it has the most aggressive neurological behavior.1,3–8 Moreover, the TDAVFs are deeply located lesions with complicated feeding arteries and draining veins, rendering them difficult in the surgical treatment. The optimal treatment strategy has remained controversial thus far.7,9–20 Endovascular therapy has become increasingly accepted for the treatment of intracranial DAVFs. But the combination of transarterial and transvenous embolization results in high obliterated rates for most of the DAVFs.7,8,10,21,22 According to the literatures,6,10,19,22–27 most authors considered TDAVF an exception and not suitable for endovascular therapy.
Correspondence to: Bin Xu, Department of Neurosurgery, Huashan Hospital, Fudan University, Urumqi Middle Road 12#, Shanghai 200040, P. R. China. Email: [email protected]; xubin_19800@163. com
ß W. S. Maney & Son Ltd 2014 DOI 10.1179/1743132814Y.0000000383
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However, some investigators recently reported several successful cases using Onyx in the management of TDAVF.28 In this paper, we reported another 26 successful cases of TDAVF treatment with Onyx.
Methods Patient population
Interventional management
A database of patient information was maintained prospectively, and clinical data were reviewed retrospectively, including medical records, radiographic reports, endovascular intervention reports, and records from office visits. During a 5-year period from January 2005 to April 2010, 40 TDAVF patients that required microsurgical or endovascular treatment were admitted to our hospital. Of these 40 patients, 13 patients underwent endovascular intervention combined with surgical treatment, 1 patient refused further treatment, and 26 patients were treated via transarterial embolization using Onyx. The mean patient age of these 26 patients was 51 years (range, 31–70 years). There was a strong male predominance, with 21 men as against 5 women.
Clinical presentation Among these 26 patients, the symptom onset time before treatment is from 2 days to 2 years. The fundamental clinical data of these patients were summarized in Table 1. Of these 26 patients, 21 patients (80.7%) had headache and/or dizziness, 2 patients (7.7%) had ataxia, 5 patients (19.2%) had pulsatile tinnitus, 1 patient (3.8%) had paralysis of oculomotor nerve, 1 patient (3.8%) had pain in face, 1 patient (3.8%) had pain in neck, 6 patients (23.1%) had weakness of limbs, 1 patient (3.8%) had lisp, 1 patient (3.8%) had dysphagia, 2 patients (7.7%) had hemiplegia, 1 patient (3.8%) had central facial palsy, and 2 patients (7.7%) had seizure. Most of the symptoms mentioned above were progressive. No etiological factors, including brain trauma, surgery, and sinus thrombosis could be identified in these patients.
Diagnosis and classification The diagnosis and classification of these patients were determined by performing computed tomography (CT) scanning, magnetic resonance imaging (MRI), and six-vessel cerebral digital subtraction angiography (DSA). Five patients with subarachnoid hemorrhage (SAH) and one patient with high-density mass in the cerebral parenchyma (intracerebral hematoma) were all confirmed by the CT scanning. The MRI demonstrated dilated and tortuous flow voids in the tentorial incisura, surface of the brainstem, and cerebellum on both T1- and T2-weighted images. The feeding arteries, fistulae, and drainage veins were analyzed in detail. Abiding by the Picard’s classification,29 7 patients were attributed to tentorial marginal type TDAVF, 13 patients to tentorial lateral
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type TDAVF, and 6 patients to tentorial medial type TDAVF. If by Borden’s classification method,3,30 8 patients were classified to Borden type II TDAVF and 18 patients were classified to Borden type III TDAVF (Table 1).
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All of the procedures were performed with general anesthesia. A 5- or 6-French Envoy guiding catheter (Cordis Endovascular, Miami Lakes, FL, USA) was introduced through the femoral artery into the external carotid artery (ECA), the internal carotid artery (ICA), or the vertebral artery (VA). Marathon microcatheters (EV3, Irvine, CA, USA) were selectively navigated to reach the distal part of the feeding arteries. Onyx was delivered via transarterial approach using the ‘reflux-hold-reinjection’ technique for better penetration into the fistula (Onyx-18 was used in the 23 patients and Onyx-34 was used in other 3 patients). For the fistula fed by bilateral arteries or the combination of carotid and vertebrobasilar arteries, the other 5-French angiographic catheter was placed in the contralateral common carotid artery or the VA. During the Onyx injection, angiography was performed through the guiding catheter or angiographic catheter to confirm the total occlusion of the fistula and undesirable embolization. The microcatheter was withdrawn when the angiogram demonstrated the complete obliteration of the fistula or the excessive reflux of Onyx. ‘Balloon assisting’ technique was employed in the conditions below. First, the balloon (HyperForm, EV3) was used in the ICA when the meningohypophyseal trunk branches (MHT) was the only appropriate approach. In this situation, the balloon could prevent Onyx reflux into the ICA and facilitate Onyx to migrate into the fistula. Second, the balloon was used in the chosen ECA branch. In this situation, the balloon could prevent Onyx reflux into other branches of the ECA and facilitate Onyx to migrate into the fistula. The interventional management of these 26 patients was also summarized in Table 1. In the subgroup of tentorial marginal type TDAVF, Onyx was injected in one session through the middle meningeal artery (MMA) in four of seven patients, including one case that was embolized while the HyperForm balloon was used in the ECA. And in other three cases, Onyx was injected through the MMA and then the MHT, including two cases that were embolized while the HyperForm balloon was used in the ICA (Fig. 1). In the subgroup of tentorial lateral type TDAVF, Onyx was injected in one session through the MMA in 8 of 13 patients. Onyx was injected through two feeding arteries in other five cases, including three cases through the occipital artery (OA) and the
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M 38
M 70
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M 42 M 52 M 55 F 57 M 43
F 66
1
2
3
4
5 6 7 8 9 10 11 12 13 14
15
16 17
18
19 20
21 22 23 24 25
26
Headache, vomit, tinnitus, myasthenia of limbs
Headache, myasthenia of limbs Headache (SAH), tinnitus, myasthenia of limbs Headache Myasthenia of limbs Vertigo, seizure Headache Headache, myasthenia of limbs
Headache
Vertigo, convulsion Headache, tinnitus
Vertigo, myasthenia of limbs Headache SAH, headache, hemiplegia, CN III SAH, headache, vomit, CNVII, IX Headache Bilateral proptosis, tinnitus Headache and cervical pain, lisp SAH, headache, vomit Ataxia, convulsion Headache, vomit, tinnitus, myasthenia of limbs Tinnitus
Headache, vertigo, ataxia, intracerebellar hemorrhage (2 years ago) Vertigo
Headache, CN V
SAH, headache, hemiplegia, CN III
Clinical presentation
OA, SCA, MMA, SPA
MMA, OA, SCA, PMA OA, SCA, MMA, SPA MMA, OA, SPA, PMA MMA, OA, PMA SPA, MMA, OA
SPA, MMA, OA MMA, OA
MMA, OA, PMA
MMA, OA, SPA, PMA MMA, OA, PMA
MMA, OA, PMA
MHT, MMA MHT, MMA, PCA MMA, MHT, PCA MMA, MHT, OA, PCA MMA, OA, PCA MMA, MHT, OA, PMA MMA, OA OA, PMA, MMA PMA, MMA OA, PMA, PCA, TCT
MMA, SPA
MHT, MMA
MHT, MMA
SPA, MMA
Feeding arteries
Leptomeningeal veins Leptomeningeal veins Leptomeningeal veins Leptomeningeal venous aneurysm Leptomeningeal and cerebellar leptomeningeal veins Leptomeningeal veins
Mesencephalic BVR (varix) to VOG, cerebellar leptomeningeal veins Cerebellar leptomeningeal venous aneurysm Mesencephalic BVR (varix) to VOG, cerebellar leptomeningeal veins Mesencephalic BVR (varix) to VOG, cerebellar leptomeningeal veins Cerebral leptomeningeal and cerebellar veins Cerebral leptomeningeal venous aneurysm
Mesencephalic BVR (venous aneurysm) to VOG, sylvian veins Spinal vein, cerebellar vein Mesencephalic BVR (varix) to VOG, sylvian veins Cerebral leptomeningeal and cerebellar veins Spinal vein, cerebellar vein Cerebral leptomeningeal and cerebellar veins Cerebral leptomeningeal and cerebellar veins Cerebral leptomeningeal venous aneurysm Cerebellar leptomeningeal venous aneurysm Cerebellar leptomeningeal veins, spinal vein Mesencephalic BVR (varix) to VOG, sylvian veins
Mesencephalic BVR (varix) to VOG, sylvian veins Mesencephalic BVR (varix) to VOG, spinal and sylvian veins Cerebellar venous aneurysm
Venous drainage
marginal type/Borden III marginal type/Borden II marginal type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden II
media media media media media
type/Borden type/Borden type/Borden type/Borden type/Borden
III III III III III Tentorial media type/Borden III
Tentorial Tentorial Tentorial Tentorial Tentorial
Tentorial media type/Borden III Tentorial media type/Borden III
Tentorial media type/Borden II
Tentorial media type/Borden III Tentorial media type/Borden II
Tentorial lateral type/Borden II
Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial
Tentorial marginal type/Borden II
Tentorial marginal type/Borden III
Tentorial marginal type/Borden II
Tentorial marginal type/Borden II
Classification
3
1 2 1 1 2
2 3
1
2 2
2
3 2 3 4 2 1 4 3 3 4
2
3
1
4
MRS when admission
SAH: Subarachnoid hemorrhage; SCA: superior cerebellar artery; MRS: modified Rankin scale; SPA: sphenopalatine artery; MMA: middle meningeal artery; MHT: meningohypophyseal trunk branches; PCA: posterior cerebral artery; OA: occipital artery; PMA: posterior meningeal artery; TCT: truncus costocervicalis; BVR: basal vein of Rosenthal; VOG, vein of Galen; CN: cranial nerve.
Sex/age (years)
Patient no.
Table 1 Patient presentation and angiographic characteristics
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Figure 1 Case 3, the patient was primary treated at the other hospital; unfortunately, a branch of external carotid artery (ECA) instead of the fistula was embolized. Then the patient was transferred to our department and received the second Onyx injection for the tentorial dural arteriovenous fistula (TDAVF). (A) Angiography of the left common carotid artery (CCA) (the lateral view). This image showed that the patient had tentorial marginal type of TDAVF, fed by the left meningohypophyseal trunk branches (MHT) (white arrow) and the left middle meningeal artery (MMA) (black arrow). (B) X-ray image before Onyx injection (lateral view). This image showed that there was a HyperForm balloon (red arrow) in the internal carotid artery (ICA), the Onyx cast (yellow arrow) in the branch of ECA (Onyx injection in the other hospital), and the microcatheter (green arrow) was navigated into the MHT. (C) X-ray image of lateral view while Onyx was injecting through the MHT. This image showed that Onyx migrated into the fistula smoothly instead of refluxing to the ICA while using the ‘balloon assisting’ technique (red arrow: the HyperForm balloon, green arrow: the tip of the microcatheter). (D) Postoperative angiography of the left CCA. The image showed that the fistula was totally obliterated.
MMA, two cases through the posterior meningeal artery (PMA) and the MMA (Fig. 2). In the subgroup of tentorial medial type TDAVF, Onyx was injected in one session through the MMA in two of six patients. Onyx was injected through two feeding arteries in other four cases, including three cases through the OA and the PMA, one case through the OA and the MMA.
(MRS) was used to grade outcomes,31 which were analyzed in terms of the MRS from preoperative to the final follow-up. All the patients underwent six-vessel angiography immediately after the operation and 3 months later, respectively. The radiological outcomes were categorized to ‘totally obliterated’, ‘sub-totally obliterated’, and ‘partially obliterated’.
Evaluation criterion
Results Immediate and short-term follow-up results
Neurological assessments were performed by neurologists, preoperatively, postoperatively, and during the follow-up period. The modified Rankin scale
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The angiographic outcomes of transarterial access embolization were summarized in Fig. 3. In the
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Figure 2 Case 22. (A) Angiography of the right internal carotid artery (ICA) (lateral view). (B) Angiography of the right ICA (frontal view). (C) Angiography of the right vertebral artery (VA) (frontal view). (D) Angiography of the right VA (lateral view). (A– D) The images showed the patient had tentorial median type of tentorial dural arteriovenous fistula (TDAVF), fed by the right occipital artery (OA), the right SCA, and the right meningohypophyseal trunk branches (MHT). (E) X-ray image (frontal view) after Onyx injection. (F) X-ray image (lateral view) after Onyx injection. (E–F) The images showed that there were Onyx casts in the fistula itself, the most proximal venous outlet, and proximal feeding arteries. (G) Postoperative angiography of the right internal carotid artery (ICA) (frontal view). (H) Postoperative angiography of the right VA (frontal view). (G–H) The images showed that the fistula was totally obliterated.
subgroup of the tentorial marginal type TDAVF, six of seven patients got angiographic cure (totally obliterated) and clinical cure (with an MRS of 0 when discharged). The other patient (patient 7) was sub-totally obliterated. However, the symptoms of cranial nerve (CN) III paralysis worsened after the operation. Fortunately, the symptoms alleviated significantly with an MRS of 1 when he was discharged. In the subgroup of the tentorial lateral type TDAVF, 7 of 13 patients got angiographic cure (totally obliterated) and clinical cure (with an MRS of 0 when they were discharged). Other six patients
still had fistula residue after the embolization. Four patients were sub-totally obliterated whose symptoms relieved significantly with an MRS of 1 when they were discharged, and two patients were partially obliterated whose symptoms relieved with an MRS of 2 when they were discharged. In the subgroup of the tentorial medial type TDAVF, four of six patients got angiographic cure (totally obliterated) and clinical cure (with an MRS of 0 when they were discharged). Other two patients were sub-totally obliterated; the symptoms were significantly relieved with an MRS of 1 when they were discharged.
Figure 3 The angiographic outcomes of transarterial access embolization. The angiographic outcome of transarterial access embolization was evaluated by modified Rankin scale (MRS). Preop is when patients were admitted into our hospital; and postop is when patients were discharged. Some curves in the plots may represent more than one patient.
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Figure 4 Vascular anatomic complexity and total obliterated rate. (A) The total obliterated rates in three different subtypes of TDAVF. The total obliterated rate was calculated within each subtype of TDAVF patients. In tentorial marginal group there are totally 7 patients; in tentorial lateral group, there are 13 patients; and in tentorial medial group, there are 6 patients. (B) The total obliterated rate in different number of feeding artery. The total obliterated rate was calculated within the same number of feeding artery. There are 8 patients with 2 feeding arteries, 10 patients with 3 feeding arteries, and 8 patients with 4 feeding arteries.
Long-time follow-up results All the patients underwent a follow-up of the DSA at 3 months after the embolization. And then they underwent the follow-up at the outpatient department or by telephone interview, for a mean duration of 2.9 years (range, 9 months to 5.3 years). All the patients had resumed their normal activities. No fistula recurrence was found in the DSA at 3 months after the embolization. There was no rehemorrhage or recurrence of the previous symptoms during the follow-up.
Complications There was no mortality and no new permanent neurological deterioration. The symptoms due to the paralysis of CN III in patient 7 were more severe immediately after the operation. However, the symptoms significantly relieved with an MRS of 1 when he was discharged. Microcatheter retention was one of the technique complications as reported, which did not happen in our series.
Discussion Venous drainage of the TDAVF Venous drainages vary greatly and depend on the tentorial location of the fistula; however, they typically drain into deep cortical and leptomeningeal veins.5 It is known that an aggressive neurological course, defined as progressive focal neurological deficit or hemorrhage, is much more frequently observed in lesions of the petrosal or straight sinus, in the fistula with leptomeningeal venous drainage, in variceal or aneurysmal venous dilations, or in Galenic drainage.1,34 The TDAVF patients, as a result of their venous drainages, commonly have
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intracranial hemorrhage or progressive neurological deficits.1,5,18,35,36 Therefore, prompt treatments are a must for the TDAVF patients.
Vascular anatomic complexity and obliterated rate In the subgroup of tentorial marginal type TDAVF, six of seven patients (85.7%) had the fistula totally obliterated. In the subgroup of tentorial lateral type TDAVF, 7 of 13 patients (53.8%) had the fistula totally obliterated. In the subgroup of tentorial medial type TDAVF, four of six patients (66.7%) had the fistula totally obliterated. Our study showed that the tentorial marginal type TDAVF had less feeding arteries than those of other two types. The fistulas of the tentorial lateral type TDAVF are always superficial but more diffuse than those of other two types. For the tentorial medial type TDAVF, the feeding arteries are more torturous and longer, making it quite difficult to catheterize. Therefore, the tentorial marginal type TDAVF has the highest angiographic obliterated rate than that of other two types (Fig. 4A). By analyzing the total 26 patients, we found that the total obliterated rate is decreased with the increase of feeding artery number (Fig. 4B).
The TDAVF treatment strategy Various treatments have been assessed regarding TDAVF, including surgical excision of the fistula, transarterial or transvenous embolization, and radiosurgery. The strategies mentioned above can be used separately or in a combination.5,7,32,35,37 The surgical treatment for TDAVF is always difficult because of the deep location and the
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Figure 5 Case 10. (A) Angiography of the left external carotid artery (ECA) (the lateral view). (B) Angiography of the left ECA (the frontal view). (A, B) The images showed that the patient had tentorial lateral type of tentorial dural arteriovenous fistula (TDAVF), fed by the left occipital artery (OA) and the left middle meningeal artery (MMA). (C) Microcatheter angiogram before Onyx injection through the left OA. (D) Microcatheter angiogram before Onyx injection through the left MMA. (C, D) We injected Onyx through the left OA firstly, but the fistula could not be completely obliterated. Then we injected Onyx through the left MMA. (E, F) Postoperative angiography of the left ECA. The image showed that the fistula was totally obliterated.
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surrounding vital structures, such as the deep venous system.32,38 Complete excision of the fistula must be confirmed by intra-operative angiography or intraoperative Doppler ultrasound monitoring.38–40 Thus, the surgical treatment is difficult, complex, and risky. Treatment using the radiosurgical strategy has been reported to be effective, but the risk of hemorrhage remains until the complete obliteration is achieved for 1–2 years.18,41 Both strategies have limitations. If endovascular embolization could achieve the same good effect as the surgical treatment does, definitely, endovascular embolization would be the optimal treatment because it is simpler and safer than the surgical treatment. In recent years, with the advances in the technique and devices, as well as our understanding of the vascular anatomic characteristic of TDAVF, some authors have described successful cases with endovascular treatment via transarterial approach, transvenous approach, or a combination of both. Transvenous embolization remains a safe and effective option for the treatment of many intracranial DAVFs.42–44 However, clearly transvenous approach is not suitable for TDAVF treatment, since majority of TDAVF patients have leptomeningeal venous drainage, which is considered to be impossible for transvenous approach.
perform a control angiogram during Onyx injection. Additionally, we used the ‘balloon assisting’ technique, which brought promising results to the three patients as shown in Table 1. We found the ‘balloon assisting’ technique is beneficial to Onyx injection in the conditions mentioned above.
The feasibility of using Onyx to treat TDAVF
Conflicts of interest The authors declare no conflicts of interest concerning the materials or methods used in this study or the findings specified in this paper. And we have no financial disclosure for this study.
Effective treatment requires precise target embolization, including the fistula itself and the most proximal venous outlet. The microcatheter should be navigated into or close to fistula. The ‘reflux-hold-reinjection’ technique should also be used in order to guarantee complete fistula obliteration. According to our experience, the tortuosity, the diameter, and the length of the feeding arteries, and the distance between the position of the microcatheter tip and the fistula should be considered while choosing the appropriate approach (Fig. 5). The importance of occluding the proximal recipient veins cannot be overemphasized, and the potential danger of occluding more distal veins should be considered, which can redirect the blood flow and cause new clinical symptoms. According to our clinical practice, excessive reflux should be avoided. As it could cause difficulty in microcatheter retrieval, which may increase the risk of vessel rupture and microcatheter retention, and further increase the risk of thromboembolic events and occlusion of the normal branches. Thus excessive reflux may eventually increase the risk of cerebral infraction and deficit of cranial nerves. To avoid inappropriate migration of the Onyx, we used the routine ‘double catheter’ technique as reported previously.32,33 Briefly, in order to monitor Onyx penetration, second catheter was used to
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Conclusion Our study demonstrated that if performed by experienced neurosurgeons, treating TDAVF via transarterial approach using Onyx might be a safe and feasible practice. When catheterization is possible, a high obliterated rate can be achieved. Among three subtypes of TDAVF, which share different vascular anatomic characteristics, the tentorial marginal type of TDAVF has the higher angiographic obliterated rate than the other two types. Our clinical practice implies that Onyx injection with the assistance of ‘double catheter’ technique and ‘balloon assisting’ technique can be very helpful in some of the cases.
Disclaimer Statements Contributors All the authors joined the design, perform, analysis, and draft of the paper. Funding None.
Ethics approval All procedures were approved by the Ethics Committee for Human Experiments of the Fudan University.
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iovenous fistulae: part 2. Aggressive lesions. Int Neuroradiol. 1997;3:303–11. Hoh BL, Choudhri TF, Connolly ES, Solomon RA. Surgical management of high-grade intracranial dural arteriovenous fistulas: leptomeningeal venous disruption without nidus excision. Neurosurgery. 1998;42:796–805. Lasjaunias P, Lopez-Ibor L, Abanou A, Halimi P. Radiological anatomy of the vascularization of cranial dural arteriovenous malformations. Anat Clin. 1984;6:87–99. Lucas CP, De Oliveira E, Tedeschi H, Siqueira M, Lourenzi M, Piske RL, et al. Sinus skeletonization: a treatment for dural arteriovenous malformations of the tentorial apex. J Neurosurg. 1996;84:514–7. Lucas CP, Zabramski JM, Spetzler RF, Jazobowitz R. Treatment for intracranial dural arteriovenous malformations: a meta-analysis from the English language literature. Neurosurgery. 1997;46:1119–32. Malek AM, Halbach VV, Hignshida RT, Phatouros CC, Meyers PM, Dowd CF. Treatment of dural arteriovenous malformations and fistulas. Neurosurg Clin N Am. 2000;11:147–66. Pierot L, Chiras J, Meder JF, Rose M, Rivierez M, Marsault C. Dural arteriovenous fistulas of the posterior fossa draining into subarachnoid veins. AJNR Am J Neuroradiol. 1992;13:315–23. Ray D, Raymond J. The role of transvenous embolization in the treatment of intracranial dural arteriovenous fistulas. Neurosurgery. 1997;40:1133–44. Ricolfi F, Manelfe C, Meder JF, Arrue´ P, Decq P, Brugie´res P, et al. Intracranial dural arteriovenous fistulae with perimedullary venous draining: anatomical, clinical and therapeutic considerations. Neuroradiology. 1999;41:803–12. Shin M, Kurita H, Tago M, Kirino T. Stereotactic radiosurgery for tentorial dura arteriovenous fistulas draining into the vein of Galen: report of two cases. Neurosurgery. 2000;46:730–4. Sundt TM, Piepgras DG. The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg. 1983;59:32–9. Thompson BG, Doppman JL, Oldfield EH. Treatment of cranial dural arteriovenous fistulae by interruption of leptomeningeal venous drainage. J Neurosurg. 1994;80:617–23. Halbach VV, Higashida RT, Hieshima GB, Wilson CB, Hardin CW, Kwan E. Treatment of dural fistulas involving the deep cerebral venous system. AJNR Am J Neuroradiol. 1989;10:393–9. Tomak PR, Cloft HJ, Kaga A, Cawley CM, Dion J, Barrow DL. Evolution of the management of tentorial dural arteriovenous malformations. Neurosurgery. 2003;52:750–62. 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. Goto K, Sidipratomo P, Ogata N, Inoue T, Matsuno H. Combining endovascular and neurosurgical treatments of highrisk dural arteriovenous fistulas in the lateral sinus and the confluence of the sinuses. J Neurosurg. 1999;90:289–99. Kattner KA, Roth TC, Giannotta SL. Cranial base approaches for the surgical treatment of aggressive posterior fossa dural arteriovenous fistulae with leptomeningeal drainage: report of four technical cases. Neurosurgery. 2002;50:1156–61. Kiyosue H, Hori Y, Okahara M, Tanoue S, Sagara Y, Matsumoto S, et al. Treatment of intracranial dural arteriovenous fistulas: current strategies based on location and hemodynamics, and alternative techniques of transcatheter embolization. Radiographics. 2004;24:1637–53. Zhang JC, Dion J, Barrow DL. Surgical treatment of intracranial dural arteriovenous fistulas. In: Lawton
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MT, Higashida RT, Gress DR, editors. Controversies in neurological surgery: neurovascular diseases. New York: Thieme Medical Publishers; 2006. p. 150–6. Pierot L, Kadziolka K, Litre F, Rousseaux P. Combined treatment of brain AVMs with use of Onyx embolization followed by radiosurgery. AJNR Am J Neuroradiol. 2013;34(7):1395–400. Picard L, Bracard S, Islak C, Roy D, Moreno A, Marchal JC, et al. Dural fistulae of the tentorium cerebelli: radioanatomical, clinical and therapeutic considerations. J Neuroradiol. 1990;17:161–81. Davies MA, TerBrugge K, Willinsky R, Coyne T, Saleh J, Wallace MC. The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg. 1996;85:830–7. Swieten JC, Koudstaal PJ, Visser MC, Schouten HJ, van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988;19:604–7. Lawton MT, Sanchez-Mejia RO, Pham D, Tan J, Halbach VV. Tentorial dural arteriovenous fistulae: operative strategies and microsurgical results for six types. Neurosurgery. 2008;62:110– 25. Huang Q, Xu Y, Hong B, Li Q, Zhao W, Liu J. Use of Onyx in the management of tentorial dural arteriovenous fistula. Neurosurgery. 2009;65:287–93 Brown RD Jr., 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. Deasy NP, Gholkar AR, Cox TC, Jeffree MA. Tentorial dural arteriovenous fistulae: endovascular treatment with transvenous coil embolization. Neuroradiology. 1999;41:308–12. King WA, Martin NA. Intracerebral hemorrhage due to dural arteriovenous malformations and fistulae. Neurosurg Clin N Am. 1992;3:577–90. Nogueira RG, Dabus G, Rabinov JD, Eskey CJ, Ogilvy CS, Hirsch JA, et al. Preliminary experience with Onyx embolization for the treatment of intracranial dural arteriovenous fistulas. AJNR Am J Neuroradiol. 2008;29:91–7. Abrahams JM, Bagley LJ, Flamm ES, Hurst RW, Sinson GP. Alternative management considerations for ethmoidal dural arteriovenous fistulas. Surg Neurol. 2002;58:410–6. Fujita A, Tamaki N, Nakamura M, Yasuo K, Morikawa M. A tentorial dural arteriovenous fistula successfully treated with interruption of leptomeningeal venous drainage using microvascular Doppler sonography: case report. Surg Neurol. 2001;56:56–61. 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. Matsushige T, Nakaoka M, Ohta K, Yahara K, Okamoto H, Kurisu K. Tentorial dural arteriovenous malformation manifesting as trigeminal neuralgia treated by stereotactic radiosurgery: a case report. Surg Neurol. 2006;66:519–23. Halbach VV, Higashida RT, Hieshima GB, Mehringer CM, Hardin CW. Transvenous embolization of dural fistulas involving the transverse and sigmoid sinuses. AJNR Am J Neuroradiol. 1989;10:385–92. Malek AM, Halbach VV, Dowd CF, Higashida RT. Diagnosis and treatment of dural arteriovenous fistulas. Neuroimaging Clin N Am. 1998;8:445–68. Shi ZS, Ziegler J, Gonzalez NR, Feng L, Tateshima S, Jahan R, et al. Transarterial embolization of clival dural arteriovenous fistula using liquid embolic agents. Neurosurgery. 2008;62:408– 15.
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Department of Neurosurgery, Changshu First People Hospital, Suzhou University, P. R. China, 2Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, P. R. China, 3Department of Neurosurgery, Deji Hospital, Shanghai, P. R. China Objective: In this study, based on clinical presentation and angiographic findings, we try to investigate the possibility to do transarterial embolization using Onyx to treat tentorial dural arteriovenous fistula (TDAVF). Particular attention will be given to the relationship between vascular anatomic characteristics and clinical management. Methods: We retrospectively reviewed the clinical and radiologic data of 26 patients with TDAVFs, who were treated via transarterial approach using Onyx (including three cases treating with balloon assisting) at our department from January 2005 to April 2010. Results: The total obliterated rate was 85.7, 53.8, and 66.7% in the tentorial marginal, lateral, and medial subtype, respectively. Symptoms were improved significantly in the patients whose fistulas were totally and sub-totally obliterated. The mean follow-up duration was 2.9 years. After operation, patients’ symptom was dramatically improved indicated by the decrease of individual modified Rankin scale (MRS). Only one patient suffered from temporary paralysis of cranial nerve (CN) III. All 26 patients were clinically stable and without any relapsed, increased, or new symptoms. All patients had resumed their normal activities until the latest follow-up. Conclusion: Treating the TDAVF via transarterial approach using Onyx maybe a feasible clinical practice. The fistula obliterated rate is highly related to the anatomic characteristic, and high complete obliterated rate can be achieved. Our preliminary results showed that Onyx injection with ‘balloon assisting’ technique can be helpful in some of the cases.
Keywords: Tentorial, Dural arteriovenous fistula, Onyx
Abbreviations
Background
TDAVF, tentorial dural arteriovenous fistula; ECA external carotid artery; M male; F female; SAH subarachnoid hemorrhage; CN cranial nerve; SPA sphenopalatine artery; MHT meningohypophyseal trunk branches; MMA middle meningeal artery; OA occipital artery; PMA posterior meningeal artery; PCA posterior cerebral artery; TCT truncus costocervicalis; BVR basal vein of Rosenthal; VOG vein of Galen; ICA internal carotid artery; CT computed tomography; MRI magnetic resonance imaging; DSA digital subtraction angiography; MRS modified Rankin scale.
Tentorial dural arteriovenous fistula (TDAVF) is a relatively rare lesion, accounting for 4–8.4% of all the intracranial DAVFs.1,2 However, 97% of the patients have hemorrhage or progressive focal neurological deficits because it has the most aggressive neurological behavior.1,3–8 Moreover, the TDAVFs are deeply located lesions with complicated feeding arteries and draining veins, rendering them difficult in the surgical treatment. The optimal treatment strategy has remained controversial thus far.7,9–20 Endovascular therapy has become increasingly accepted for the treatment of intracranial DAVFs. But the combination of transarterial and transvenous embolization results in high obliterated rates for most of the DAVFs.7,8,10,21,22 According to the literatures,6,10,19,22–27 most authors considered TDAVF an exception and not suitable for endovascular therapy.
Correspondence to: Bin Xu, Department of Neurosurgery, Huashan Hospital, Fudan University, Urumqi Middle Road 12#, Shanghai 200040, P. R. China. Email: [email protected]; xubin_19800@163. com
ß W. S. Maney & Son Ltd 2014 DOI 10.1179/1743132814Y.0000000383
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However, some investigators recently reported several successful cases using Onyx in the management of TDAVF.28 In this paper, we reported another 26 successful cases of TDAVF treatment with Onyx.
Methods Patient population
Interventional management
A database of patient information was maintained prospectively, and clinical data were reviewed retrospectively, including medical records, radiographic reports, endovascular intervention reports, and records from office visits. During a 5-year period from January 2005 to April 2010, 40 TDAVF patients that required microsurgical or endovascular treatment were admitted to our hospital. Of these 40 patients, 13 patients underwent endovascular intervention combined with surgical treatment, 1 patient refused further treatment, and 26 patients were treated via transarterial embolization using Onyx. The mean patient age of these 26 patients was 51 years (range, 31–70 years). There was a strong male predominance, with 21 men as against 5 women.
Clinical presentation Among these 26 patients, the symptom onset time before treatment is from 2 days to 2 years. The fundamental clinical data of these patients were summarized in Table 1. Of these 26 patients, 21 patients (80.7%) had headache and/or dizziness, 2 patients (7.7%) had ataxia, 5 patients (19.2%) had pulsatile tinnitus, 1 patient (3.8%) had paralysis of oculomotor nerve, 1 patient (3.8%) had pain in face, 1 patient (3.8%) had pain in neck, 6 patients (23.1%) had weakness of limbs, 1 patient (3.8%) had lisp, 1 patient (3.8%) had dysphagia, 2 patients (7.7%) had hemiplegia, 1 patient (3.8%) had central facial palsy, and 2 patients (7.7%) had seizure. Most of the symptoms mentioned above were progressive. No etiological factors, including brain trauma, surgery, and sinus thrombosis could be identified in these patients.
Diagnosis and classification The diagnosis and classification of these patients were determined by performing computed tomography (CT) scanning, magnetic resonance imaging (MRI), and six-vessel cerebral digital subtraction angiography (DSA). Five patients with subarachnoid hemorrhage (SAH) and one patient with high-density mass in the cerebral parenchyma (intracerebral hematoma) were all confirmed by the CT scanning. The MRI demonstrated dilated and tortuous flow voids in the tentorial incisura, surface of the brainstem, and cerebellum on both T1- and T2-weighted images. The feeding arteries, fistulae, and drainage veins were analyzed in detail. Abiding by the Picard’s classification,29 7 patients were attributed to tentorial marginal type TDAVF, 13 patients to tentorial lateral
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type TDAVF, and 6 patients to tentorial medial type TDAVF. If by Borden’s classification method,3,30 8 patients were classified to Borden type II TDAVF and 18 patients were classified to Borden type III TDAVF (Table 1).
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All of the procedures were performed with general anesthesia. A 5- or 6-French Envoy guiding catheter (Cordis Endovascular, Miami Lakes, FL, USA) was introduced through the femoral artery into the external carotid artery (ECA), the internal carotid artery (ICA), or the vertebral artery (VA). Marathon microcatheters (EV3, Irvine, CA, USA) were selectively navigated to reach the distal part of the feeding arteries. Onyx was delivered via transarterial approach using the ‘reflux-hold-reinjection’ technique for better penetration into the fistula (Onyx-18 was used in the 23 patients and Onyx-34 was used in other 3 patients). For the fistula fed by bilateral arteries or the combination of carotid and vertebrobasilar arteries, the other 5-French angiographic catheter was placed in the contralateral common carotid artery or the VA. During the Onyx injection, angiography was performed through the guiding catheter or angiographic catheter to confirm the total occlusion of the fistula and undesirable embolization. The microcatheter was withdrawn when the angiogram demonstrated the complete obliteration of the fistula or the excessive reflux of Onyx. ‘Balloon assisting’ technique was employed in the conditions below. First, the balloon (HyperForm, EV3) was used in the ICA when the meningohypophyseal trunk branches (MHT) was the only appropriate approach. In this situation, the balloon could prevent Onyx reflux into the ICA and facilitate Onyx to migrate into the fistula. Second, the balloon was used in the chosen ECA branch. In this situation, the balloon could prevent Onyx reflux into other branches of the ECA and facilitate Onyx to migrate into the fistula. The interventional management of these 26 patients was also summarized in Table 1. In the subgroup of tentorial marginal type TDAVF, Onyx was injected in one session through the middle meningeal artery (MMA) in four of seven patients, including one case that was embolized while the HyperForm balloon was used in the ECA. And in other three cases, Onyx was injected through the MMA and then the MHT, including two cases that were embolized while the HyperForm balloon was used in the ICA (Fig. 1). In the subgroup of tentorial lateral type TDAVF, Onyx was injected in one session through the MMA in 8 of 13 patients. Onyx was injected through two feeding arteries in other five cases, including three cases through the occipital artery (OA) and the
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M 38
M 70
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M 37 M 48 M 39 M 53 M 48 M 47 M 53 M 58 F 45 F 66
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M 55 M 46
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M 42 M 52 M 55 F 57 M 43
F 66
1
2
3
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5 6 7 8 9 10 11 12 13 14
15
16 17
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19 20
21 22 23 24 25
26
Headache, vomit, tinnitus, myasthenia of limbs
Headache, myasthenia of limbs Headache (SAH), tinnitus, myasthenia of limbs Headache Myasthenia of limbs Vertigo, seizure Headache Headache, myasthenia of limbs
Headache
Vertigo, convulsion Headache, tinnitus
Vertigo, myasthenia of limbs Headache SAH, headache, hemiplegia, CN III SAH, headache, vomit, CNVII, IX Headache Bilateral proptosis, tinnitus Headache and cervical pain, lisp SAH, headache, vomit Ataxia, convulsion Headache, vomit, tinnitus, myasthenia of limbs Tinnitus
Headache, vertigo, ataxia, intracerebellar hemorrhage (2 years ago) Vertigo
Headache, CN V
SAH, headache, hemiplegia, CN III
Clinical presentation
OA, SCA, MMA, SPA
MMA, OA, SCA, PMA OA, SCA, MMA, SPA MMA, OA, SPA, PMA MMA, OA, PMA SPA, MMA, OA
SPA, MMA, OA MMA, OA
MMA, OA, PMA
MMA, OA, SPA, PMA MMA, OA, PMA
MMA, OA, PMA
MHT, MMA MHT, MMA, PCA MMA, MHT, PCA MMA, MHT, OA, PCA MMA, OA, PCA MMA, MHT, OA, PMA MMA, OA OA, PMA, MMA PMA, MMA OA, PMA, PCA, TCT
MMA, SPA
MHT, MMA
MHT, MMA
SPA, MMA
Feeding arteries
Leptomeningeal veins Leptomeningeal veins Leptomeningeal veins Leptomeningeal venous aneurysm Leptomeningeal and cerebellar leptomeningeal veins Leptomeningeal veins
Mesencephalic BVR (varix) to VOG, cerebellar leptomeningeal veins Cerebellar leptomeningeal venous aneurysm Mesencephalic BVR (varix) to VOG, cerebellar leptomeningeal veins Mesencephalic BVR (varix) to VOG, cerebellar leptomeningeal veins Cerebral leptomeningeal and cerebellar veins Cerebral leptomeningeal venous aneurysm
Mesencephalic BVR (venous aneurysm) to VOG, sylvian veins Spinal vein, cerebellar vein Mesencephalic BVR (varix) to VOG, sylvian veins Cerebral leptomeningeal and cerebellar veins Spinal vein, cerebellar vein Cerebral leptomeningeal and cerebellar veins Cerebral leptomeningeal and cerebellar veins Cerebral leptomeningeal venous aneurysm Cerebellar leptomeningeal venous aneurysm Cerebellar leptomeningeal veins, spinal vein Mesencephalic BVR (varix) to VOG, sylvian veins
Mesencephalic BVR (varix) to VOG, sylvian veins Mesencephalic BVR (varix) to VOG, spinal and sylvian veins Cerebellar venous aneurysm
Venous drainage
marginal type/Borden III marginal type/Borden II marginal type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden III lateral type/Borden II
media media media media media
type/Borden type/Borden type/Borden type/Borden type/Borden
III III III III III Tentorial media type/Borden III
Tentorial Tentorial Tentorial Tentorial Tentorial
Tentorial media type/Borden III Tentorial media type/Borden III
Tentorial media type/Borden II
Tentorial media type/Borden III Tentorial media type/Borden II
Tentorial lateral type/Borden II
Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial Tentorial
Tentorial marginal type/Borden II
Tentorial marginal type/Borden III
Tentorial marginal type/Borden II
Tentorial marginal type/Borden II
Classification
3
1 2 1 1 2
2 3
1
2 2
2
3 2 3 4 2 1 4 3 3 4
2
3
1
4
MRS when admission
SAH: Subarachnoid hemorrhage; SCA: superior cerebellar artery; MRS: modified Rankin scale; SPA: sphenopalatine artery; MMA: middle meningeal artery; MHT: meningohypophyseal trunk branches; PCA: posterior cerebral artery; OA: occipital artery; PMA: posterior meningeal artery; TCT: truncus costocervicalis; BVR: basal vein of Rosenthal; VOG, vein of Galen; CN: cranial nerve.
Sex/age (years)
Patient no.
Table 1 Patient presentation and angiographic characteristics
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Figure 1 Case 3, the patient was primary treated at the other hospital; unfortunately, a branch of external carotid artery (ECA) instead of the fistula was embolized. Then the patient was transferred to our department and received the second Onyx injection for the tentorial dural arteriovenous fistula (TDAVF). (A) Angiography of the left common carotid artery (CCA) (the lateral view). This image showed that the patient had tentorial marginal type of TDAVF, fed by the left meningohypophyseal trunk branches (MHT) (white arrow) and the left middle meningeal artery (MMA) (black arrow). (B) X-ray image before Onyx injection (lateral view). This image showed that there was a HyperForm balloon (red arrow) in the internal carotid artery (ICA), the Onyx cast (yellow arrow) in the branch of ECA (Onyx injection in the other hospital), and the microcatheter (green arrow) was navigated into the MHT. (C) X-ray image of lateral view while Onyx was injecting through the MHT. This image showed that Onyx migrated into the fistula smoothly instead of refluxing to the ICA while using the ‘balloon assisting’ technique (red arrow: the HyperForm balloon, green arrow: the tip of the microcatheter). (D) Postoperative angiography of the left CCA. The image showed that the fistula was totally obliterated.
MMA, two cases through the posterior meningeal artery (PMA) and the MMA (Fig. 2). In the subgroup of tentorial medial type TDAVF, Onyx was injected in one session through the MMA in two of six patients. Onyx was injected through two feeding arteries in other four cases, including three cases through the OA and the PMA, one case through the OA and the MMA.
(MRS) was used to grade outcomes,31 which were analyzed in terms of the MRS from preoperative to the final follow-up. All the patients underwent six-vessel angiography immediately after the operation and 3 months later, respectively. The radiological outcomes were categorized to ‘totally obliterated’, ‘sub-totally obliterated’, and ‘partially obliterated’.
Evaluation criterion
Results Immediate and short-term follow-up results
Neurological assessments were performed by neurologists, preoperatively, postoperatively, and during the follow-up period. The modified Rankin scale
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The angiographic outcomes of transarterial access embolization were summarized in Fig. 3. In the
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Figure 2 Case 22. (A) Angiography of the right internal carotid artery (ICA) (lateral view). (B) Angiography of the right ICA (frontal view). (C) Angiography of the right vertebral artery (VA) (frontal view). (D) Angiography of the right VA (lateral view). (A– D) The images showed the patient had tentorial median type of tentorial dural arteriovenous fistula (TDAVF), fed by the right occipital artery (OA), the right SCA, and the right meningohypophyseal trunk branches (MHT). (E) X-ray image (frontal view) after Onyx injection. (F) X-ray image (lateral view) after Onyx injection. (E–F) The images showed that there were Onyx casts in the fistula itself, the most proximal venous outlet, and proximal feeding arteries. (G) Postoperative angiography of the right internal carotid artery (ICA) (frontal view). (H) Postoperative angiography of the right VA (frontal view). (G–H) The images showed that the fistula was totally obliterated.
subgroup of the tentorial marginal type TDAVF, six of seven patients got angiographic cure (totally obliterated) and clinical cure (with an MRS of 0 when discharged). The other patient (patient 7) was sub-totally obliterated. However, the symptoms of cranial nerve (CN) III paralysis worsened after the operation. Fortunately, the symptoms alleviated significantly with an MRS of 1 when he was discharged. In the subgroup of the tentorial lateral type TDAVF, 7 of 13 patients got angiographic cure (totally obliterated) and clinical cure (with an MRS of 0 when they were discharged). Other six patients
still had fistula residue after the embolization. Four patients were sub-totally obliterated whose symptoms relieved significantly with an MRS of 1 when they were discharged, and two patients were partially obliterated whose symptoms relieved with an MRS of 2 when they were discharged. In the subgroup of the tentorial medial type TDAVF, four of six patients got angiographic cure (totally obliterated) and clinical cure (with an MRS of 0 when they were discharged). Other two patients were sub-totally obliterated; the symptoms were significantly relieved with an MRS of 1 when they were discharged.
Figure 3 The angiographic outcomes of transarterial access embolization. The angiographic outcome of transarterial access embolization was evaluated by modified Rankin scale (MRS). Preop is when patients were admitted into our hospital; and postop is when patients were discharged. Some curves in the plots may represent more than one patient.
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Figure 4 Vascular anatomic complexity and total obliterated rate. (A) The total obliterated rates in three different subtypes of TDAVF. The total obliterated rate was calculated within each subtype of TDAVF patients. In tentorial marginal group there are totally 7 patients; in tentorial lateral group, there are 13 patients; and in tentorial medial group, there are 6 patients. (B) The total obliterated rate in different number of feeding artery. The total obliterated rate was calculated within the same number of feeding artery. There are 8 patients with 2 feeding arteries, 10 patients with 3 feeding arteries, and 8 patients with 4 feeding arteries.
Long-time follow-up results All the patients underwent a follow-up of the DSA at 3 months after the embolization. And then they underwent the follow-up at the outpatient department or by telephone interview, for a mean duration of 2.9 years (range, 9 months to 5.3 years). All the patients had resumed their normal activities. No fistula recurrence was found in the DSA at 3 months after the embolization. There was no rehemorrhage or recurrence of the previous symptoms during the follow-up.
Complications There was no mortality and no new permanent neurological deterioration. The symptoms due to the paralysis of CN III in patient 7 were more severe immediately after the operation. However, the symptoms significantly relieved with an MRS of 1 when he was discharged. Microcatheter retention was one of the technique complications as reported, which did not happen in our series.
Discussion Venous drainage of the TDAVF Venous drainages vary greatly and depend on the tentorial location of the fistula; however, they typically drain into deep cortical and leptomeningeal veins.5 It is known that an aggressive neurological course, defined as progressive focal neurological deficit or hemorrhage, is much more frequently observed in lesions of the petrosal or straight sinus, in the fistula with leptomeningeal venous drainage, in variceal or aneurysmal venous dilations, or in Galenic drainage.1,34 The TDAVF patients, as a result of their venous drainages, commonly have
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intracranial hemorrhage or progressive neurological deficits.1,5,18,35,36 Therefore, prompt treatments are a must for the TDAVF patients.
Vascular anatomic complexity and obliterated rate In the subgroup of tentorial marginal type TDAVF, six of seven patients (85.7%) had the fistula totally obliterated. In the subgroup of tentorial lateral type TDAVF, 7 of 13 patients (53.8%) had the fistula totally obliterated. In the subgroup of tentorial medial type TDAVF, four of six patients (66.7%) had the fistula totally obliterated. Our study showed that the tentorial marginal type TDAVF had less feeding arteries than those of other two types. The fistulas of the tentorial lateral type TDAVF are always superficial but more diffuse than those of other two types. For the tentorial medial type TDAVF, the feeding arteries are more torturous and longer, making it quite difficult to catheterize. Therefore, the tentorial marginal type TDAVF has the highest angiographic obliterated rate than that of other two types (Fig. 4A). By analyzing the total 26 patients, we found that the total obliterated rate is decreased with the increase of feeding artery number (Fig. 4B).
The TDAVF treatment strategy Various treatments have been assessed regarding TDAVF, including surgical excision of the fistula, transarterial or transvenous embolization, and radiosurgery. The strategies mentioned above can be used separately or in a combination.5,7,32,35,37 The surgical treatment for TDAVF is always difficult because of the deep location and the
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Figure 5 Case 10. (A) Angiography of the left external carotid artery (ECA) (the lateral view). (B) Angiography of the left ECA (the frontal view). (A, B) The images showed that the patient had tentorial lateral type of tentorial dural arteriovenous fistula (TDAVF), fed by the left occipital artery (OA) and the left middle meningeal artery (MMA). (C) Microcatheter angiogram before Onyx injection through the left OA. (D) Microcatheter angiogram before Onyx injection through the left MMA. (C, D) We injected Onyx through the left OA firstly, but the fistula could not be completely obliterated. Then we injected Onyx through the left MMA. (E, F) Postoperative angiography of the left ECA. The image showed that the fistula was totally obliterated.
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surrounding vital structures, such as the deep venous system.32,38 Complete excision of the fistula must be confirmed by intra-operative angiography or intraoperative Doppler ultrasound monitoring.38–40 Thus, the surgical treatment is difficult, complex, and risky. Treatment using the radiosurgical strategy has been reported to be effective, but the risk of hemorrhage remains until the complete obliteration is achieved for 1–2 years.18,41 Both strategies have limitations. If endovascular embolization could achieve the same good effect as the surgical treatment does, definitely, endovascular embolization would be the optimal treatment because it is simpler and safer than the surgical treatment. In recent years, with the advances in the technique and devices, as well as our understanding of the vascular anatomic characteristic of TDAVF, some authors have described successful cases with endovascular treatment via transarterial approach, transvenous approach, or a combination of both. Transvenous embolization remains a safe and effective option for the treatment of many intracranial DAVFs.42–44 However, clearly transvenous approach is not suitable for TDAVF treatment, since majority of TDAVF patients have leptomeningeal venous drainage, which is considered to be impossible for transvenous approach.
perform a control angiogram during Onyx injection. Additionally, we used the ‘balloon assisting’ technique, which brought promising results to the three patients as shown in Table 1. We found the ‘balloon assisting’ technique is beneficial to Onyx injection in the conditions mentioned above.
The feasibility of using Onyx to treat TDAVF
Conflicts of interest The authors declare no conflicts of interest concerning the materials or methods used in this study or the findings specified in this paper. And we have no financial disclosure for this study.
Effective treatment requires precise target embolization, including the fistula itself and the most proximal venous outlet. The microcatheter should be navigated into or close to fistula. The ‘reflux-hold-reinjection’ technique should also be used in order to guarantee complete fistula obliteration. According to our experience, the tortuosity, the diameter, and the length of the feeding arteries, and the distance between the position of the microcatheter tip and the fistula should be considered while choosing the appropriate approach (Fig. 5). The importance of occluding the proximal recipient veins cannot be overemphasized, and the potential danger of occluding more distal veins should be considered, which can redirect the blood flow and cause new clinical symptoms. According to our clinical practice, excessive reflux should be avoided. As it could cause difficulty in microcatheter retrieval, which may increase the risk of vessel rupture and microcatheter retention, and further increase the risk of thromboembolic events and occlusion of the normal branches. Thus excessive reflux may eventually increase the risk of cerebral infraction and deficit of cranial nerves. To avoid inappropriate migration of the Onyx, we used the routine ‘double catheter’ technique as reported previously.32,33 Briefly, in order to monitor Onyx penetration, second catheter was used to
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Conclusion Our study demonstrated that if performed by experienced neurosurgeons, treating TDAVF via transarterial approach using Onyx might be a safe and feasible practice. When catheterization is possible, a high obliterated rate can be achieved. Among three subtypes of TDAVF, which share different vascular anatomic characteristics, the tentorial marginal type of TDAVF has the higher angiographic obliterated rate than the other two types. Our clinical practice implies that Onyx injection with the assistance of ‘double catheter’ technique and ‘balloon assisting’ technique can be very helpful in some of the cases.
Disclaimer Statements Contributors All the authors joined the design, perform, analysis, and draft of the paper. Funding None.
Ethics approval All procedures were approved by the Ethics Committee for Human Experiments of the Fudan University.
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