Management of Aggressive Cerebral Dural Arteriovenous Fistulae: Experience Using Endovascular Embolization 1
2
3
2
2
Rajeev Sivasankar , Raju Augustine George , Rochan Pant , Samresh Sahu , Rohit Aggarwal , and 2 Aftab Alam 1Department 2Dept
of Imaging & interventional Radiology, INHS Asvini, Mumbai 400005
of Radiodiagnosis & Interventional Radiology, Command Hospital Air Force, Bangalore-560007
3Department
of Imaging & interventional Radiology, MH (CTC), Pune, India
Journal of Vascular and Interventional Neurology, Vol. 9
Introduction The true incidence of cerebral dural arteriovenous fistulae (DAVF) is largely unknown [1]. It is estimated that these malformations account for less than 10% of all intracranial vascular malformations [2]. It is hypothesized that these fistulae develop following venous or cortical sinus thrombosis following which multiple fistulous communications develop, typically between numerous branches of the ECA, ICA, and/or vertebral artery and a venous sinus and/or intracranial veins [3]. Any intracranial venous sinus may be involved. Clinical manifestations depend upon the location and anatomy of the lesion. Various classification systems have been used to address the nature of these fistulae; however, the commonly used ones include the Borden classification [4] or the one proposed by Cognard [5]. The aggressive subtypes of DAVFs are associated with retrograde venous sinus, cortical venous, or spinal venous reflux, which lead to intracranial haemorrhage or neurological deficit [6]. Other features suggestive of the aggressiveness of DAVFs are stenosis of the draining sinus, deep venous drainage, certain locations like the anterior cranial fossa and tentorium, venous congestion and venous aneurysm, or varix, mainly in those DAVFs with direct leptomeningeal venous drainage [7]. Endovascular management is now the primary modality of treatment for all DAVFs. We wish to present our experience in treating 22 patients with 25 aggressive intracranial DAVFs using transarterial embolization with ethylene vinyl alcohol (EVOH) co-polymer or transvenous coiling aimed at occlusion of the venous drainage along with all its arterial supply.
Materials and Methods Twenty five aggressive cerebral DAVFs were treated between January 2013 and October 2016 in 22 patients
and data were retrospectively analyzed. Clinical manifestations and locations of 22 patients are shown in Table 1. There were 17 males and 5 females whose age ranged from 30 to 78 years. Five patients had a prior history of treatment for venous sinus thrombosis, one of the patients with multi-focal fistulae had exposure to high altitude for 2 years prior to being symptomatic, and one patient had a prior closed head injury. Four patients had fistulae which had angiographic features conforming to the “benign” variety (Cognard types I and IIa or Borden type I). These were managed conservatively, but patients have been kept under follow-up. All patients underwent angiography and embolization on a single plane angiography unit (Integris, Allura, Philips or Polystar T.O.P, and Siemens). Patients initially underwent a six-vessel cerebral angiogram under local anaesthesia. Patients were chosen for treatment only if angiograms revealed aggressive features (Borden types II or III). Therapeutic embolization was performed in a different session under general anaesthesia using EVOH copolymer in all of the cases except three patients. These included two patients with cavernous sinus DAVFs, which were treated using a transvenous approach and coil embolization, one case of an orbital apex DAVF which was treated using direct superior ophthalmic vein “cut-down” followed by transvenous coiling. This patient had a residual fistula on control angiogram, which was treated using a transarterial approach using EVOH co-polymer. Two of the 22 patients had multifocal fistulae, and the fistulae considered to have the most aggressive features were targeted first. The usual approach for transarterial embolization involved using a 6F common femoral arterial access and placement of a 6F guiding catheter (Envoy, Codman Neurovascular or Guider, Stryker Neurovascular) in the ECA or the verte-
Vol. 9, No. 4, pp. 22–28. Published June, 2017. All Rights Reserved by JVIN. Unauthorized reproduction of this article is prohibited Corresponding Author: Rajeev Sivasankar MD DNB FINR, Sr Adv (Rad) and Interventional Neuroradiologist, Department of Imaging and Interventional Radiology, INHS Asvini, Mumbai, India.
Sivasankar et al.
23
Table 1. S. No Location 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
Journal of Vascular and Interventional Neurology, Vol. 9
15. 16. 17. 18. 19. 20. 21. 22.
Lateral sinus Lateral sinus Orbital apex Tentorial Lateral sinus Condylar canal Mastoid emissary Lateral sinus Cavernous sinus Jugular bulb SSS Lateral sinus Cavernous sinus Parietal Cortical vein (type III) Jugular bulb Lateral sinus Cortical vein (Borden III) + Jugular bulb+ Lateral sinus Lateral sinus + Jugular bulb Tentorial Cavernous sinus Torcular & Medial transverse Lateral sinus
Headaches Visual symptoms + + + + + + + + + + + + -
Papilledema Seizures ICH Tinnitus Cognitive impairment + + + + + + + + + + + + + + + + + + + +
Neurological deficits + + + + + -
+
+
+
-
-
+ + -
+
-
+ + + -
+ -
-
-
-
+ +
+ -
+ -
bral artery. A dimethyl sulfoxide (DMSO) compatible flow guided microcatheter (Marathon or Apollo, Medtronic) was used in all cases over 0.008” microwire (Mirage, Covidien/Medtronic) or 0.012” microwire (Traxcess, Microvention) to access the artery and navigate as close to the fistulous site as possible). After suitability of microcatheter position was ascertained using microcatheter angiograms, the microcatheters were flushed using 10 cc of saline and dead space filled with 0.3 cc of DMSO. Thereafter, tantalum admixed EVOH co-polymer (Onyx, EV3/Medtronic or Squid, Emboflu) was injected using the standard “plug and push” method so as to achieve exclusion of fistulae. Sixteen out of 25 fistulae were embolized using Squid-12, while seven (including the repeat embolization for the residual orbital apex DAVF) were embolized using Onyx-18. In none of the cases, other concentrations of Squid or Onyx used. Endovascular technique for transvenous coiling involved placing a 6F guiding catheter (Envoy, Codman Neurovascular or Guider, Stryker Neurovascular) in the IJV and a 4F diagnostic H1 catheter in the ICA. A dual tip microcatheter (Echelon-10, EV3) was navigated over a 0.014” microwire (Synchro-14, Stryker Neurovascular or Traxcess-14, Microvention) via the inferior petrosal sinus to reach the cavernous sinus and further into the superior ophthalmic vein. Thereafter, multiple detachable platinum microcoils were used to achieve exclusion of the fistula. All patients were extubated postoperatively. Two patients were on short-term anticoagulation for 24 hours for post-procedural venous stasis. Patients were followed up clinically at one month, with MRI at three months and a control cerebral angiogram performed when possible at 6 months. All patients under-
went post-operative CT scans to exclude haemorrhagic procedural complications.
Results Location Based on location, nine of the 25 DAVFs (36%) occurred at the lateral sinus (transverse-sigmoid sinus), four at the jugular bulb (16%), three occurred at the cavernous sinus (12%), two each were at the cortical veins, tentorial sinus (8% each), one each occurred at the orbital apex, mastoid emissary, condylar canal, SSS, and torcula (4% each). Clinical presentation Twelve of 22 patients had headaches (54.5%), 11 had tinnitus (50%), 8 of 22 (36.3%) had cognitive impairment on mini-mental status examination, 6 of 22 (27.3%) had neurological deficits, 6 of 22 (27.3%) had visual symptoms (chemosis, proptosis, and/or exophthalmos), 5 had papilledema (22.8%), and 3 had intra cerebral haemorrhage (13.6%). In patients with lateral sinus DAVFs, four of nine (44.5%) patients had headaches and seven of nine (77.8%) had tinnitus. Those with cavernous sinus DAVFs presented with visual symptoms (3/3, 100%), neurological deficits (cranial nerve palsies in 2/3, 66.7%), or papilledema (2/3, 66.7%). Endovascular treatment results Twenty two patients in this study group had 25 fistulae embolized. In the group in which EVOH was used, of the 22 fistulae, complete occlusion on immediate post-
24
Journal of Vascular and Interventional Neurology, Vol. 9
procedural angiogram was achieved in 18 ( 81.8%) of the fistulae. Three of the fistulae had marked slow flow on immediate post-procedural angiograms (13.6%), which, however, were completely occluded on their control angiograms. Six-month control angiograms were performed in nine patients, which showed stable occlusions. One patient with multi-focal DAVFs had partial embolization of his lateral sinus fistula, which required another session of treatment using an alternate arterial pedicle (4.5%). Of the three patients who underwent transvenous coiling, two of the patients with cavernous sinus DAVFs achieved good post-procedural result (66.6%). The patient with an orbital apex DAVF, which required direct superior ophthalmic vein access and transvenous coiling, showed an initial good angiographic result but had a residual fistula on follow-up angiogram. This was treated by the transarterial route using the accessory meningeal artery. A total of 27 arteries were embolized: the middle meningeal artery in 21, the occipital artery in 2, accessory meningeal artery in 1, the ascending pharyngeal in 2, and the posterior meningeal artery in 1. The volume of EVOH injected ranged from 0.3 cc to 8 cc per procedure. The duration of injection per pedicle ranged from 20 min to 60 min. In the overall analysis of the endovascular treatment experience, all fistulae (25/25) achieved angiographic exclusion at the end of their treatment sessions. Complications Two patients developed post embolization headaches and drowsiness, which was probably due to venous stasis. This was managed with anticoagulation and recovery was uneventful. Another patient had a groin hematoma which was managed conservatively. Representative cases Case 1—A 62-year-old male presented with history of headaches and gradually progressive weakness of both upper and lower limbs since one year. On examination, patient had neurocognitive decline on mini-mental status examination, reduced power (grade III/V in both upper limbs and II/V both lower limbs). His MRI revealed prominent and dilated veins in both cerebral hemispheres and around the brain stem. Cerebral angiogram [Figure 1(a)] revealed aggressive high flow dural fistulae involving his right lateral sinus (single arrow) and jugular bulb (double arrow) with reflux into his venous sinuses and deep veins [Figure 1(b)]. Reflux into the spinal perimedullary venous system accounted for his limb weakness. Marked cortical venous congestion [Figure 1(c)] was present in both cerebral hemispheres.
The right lateral sinus high flow dural AVF was treated in the first session using transarterial approach via the middle meningeal artery and injection of Onyx-18. Post embolization angiogram revealed a small residual fistula present in the medial aspect of the right transverse sinus [Figure 1(d)] and high flow right jugular bulb fistula [Figure 1(e)]. The jugular bulb fistula was treated using via the Ascending pharyngeal artery and Onyx injection. Complete exclusion of fistula was achieved [Figure 1(f)–(h)]. Thereafter, the residual fistula in the medial aspect of the transverse sinus DAVF was treated using the posterior meningeal artery and embolization done using Onyx-18 [Figure 1(i)–(l)]. Complete exclusion of the fistulae was obtained and the patient made a full recovery. Case 2—Seventy-two-year-old man with a past history of head injury 25 years ago presented with progressively increasing swelling behind his left ear since seven years, which were associated with headaches. Examination revealed a pulsatile, soft swelling over his mastoid region. There was history of having been taken up for embolization at some other centre five years ago, and fistula partially embolized. Cerebral angiogram [Figure 2(a)] revealed a high flow mastoid emissary fistula supplied by branches of the middle meningeal artery and occipital artery (single arrow). There were marked cortical venous reflux and presence of venous aneurysms (double arrows). Transarterial approach was used via the middle meningeal artery [Figure 2(b)] and fistula embolized using Squid-12. Post embolization angiogram revealed complete exclusion of the fistula [Figure 2(c) and (d)]. Case 3—Sixty-five-year-old lady presented with headaches, bilateral chemosis, and proptosis for 4 months. MRI revealed a small old right temporal bleed. Cerebral angiogram showed a high flow left condylar canal dural AVF with extensive reflux into both hemispheres [Figure 3(a)]. Patient was taken for endovascular treatment via the transvenous route [Figure 3(b)]; however, platinum microcoils would not take the desired shape of the pouch and a transarterial route via the ascending pharyngeal artery used with Squid embolization [Figure 3(c)]. Post-embolization angiogram shows exclusion of the fistula with EVOH cast at the condylar canal [Figure 3(d) and (e)].
Discussion Cerebral DAVFs are uncommon lesions which account for about 10% of intracranial vascular malformations [2]. These fistulae occur as direct connections between
Sivasankar et al.
25
Journal of Vascular and Interventional Neurology, Vol. 9
Figure 1. Multi-focal DAVFs. (a) Right ECA angiogram AP projection shows high flow DAVF at the right lateral sinus
(single arrow) and another at the right jugular bulb (double arrow). the sinus is occluded. (b) Right ECA angiogram lateral projection demonstrates the marked reflux into venous sinuses and deep veins. (c) There was associated reflux into the spinal perimedullary venous system which accounted for his limb weakness. Marked cortical venous congestion was present in both cerebral hemispheres. (d) Post embolization right CCA angiogram Towne projection shows jugular bulb fistula (single arrow) and residual right transverse sinus fistula with Onyx cast (double arrow) occupying most of the right transverse sinus. (e) Right CCA angiogram lateral projection shows the jugular bulb fistula (arrow) supplied by the Neuromeningeal trunk. (f) Marathon microcatheter (arrow) navigated into the Neuromeningeal trunk and a 4 mm x 15 mm compliant balloon placed in the ipsilateral vertebral artery for protection (double arrows). Onyx cast (white star) is seen in the right transverse sinus from the first session of embolization. (g) Post embolization ECA angiogram shows complete exclusion of jugular bulb DAVF with residual fistula at the lateral sinus fed by branches of the occipital artery. (h) Onyx cast seen in the right transverse sinus (single arrow) and right jugular bulb (double arrows) at the end of the second session of embolization. (i) and (j) Right VA angiograms in Towne and lateral projections show supply to the right transverse sinus fistula from posterior meningeal artery (arrow). (k) Microcatheter navigated into the posterior meningeal artery. (l) Post embolization right VA angiogram shows complete exclusion of the lateral sinus fistula.
one or more arteries that supply the dura mater and are usually acquired conditions. Current evidence favors their occurrence as explained by the three stage hypothesis, wherein the initial event is that of venous sinus thrombosis, following which nascent fistulae develop on the walls of the sinus between the dural arteries and the venous tributaries as a result of the action of various
angiogenetic and inflammatory factors. These fistulous connections enlarge over time and attempt to recanalize the sinus. The presence of increased venous back pressure, stenosis, or occlusion results in reflux of the now arterialized blood into other sinuses or leptomeningeal veins [8–10].
26
Journal of Vascular and Interventional Neurology, Vol. 9
Figure 2. (a) Mastoid emissary DAVF. Single arrow: point of fistula supplied by branches of the MMA and occipital artery. Double arrow: venous aneurysms and the marked cortical venous reflux. (b) Mastoid emissary DAVF. Single arrow: microcatheter navigated close to the fistulous point. (c) and (d) Squid used as embolic agent. Post embolization ECA angiogram lateral projection shows complete exclusion of fistula.
There is a direct correlation between the degree of venous reflux and the incidence of cerebral haemorrhage, which mandates early management of aggressive cerebral dural AVFs [4,5]. The overall annual risk of haemorrhage in patients with intracranial dAVFs is 1.8%, with a case fatality rate of 20% with haemorrhage [11]. The aim of management is to occlude the fistulous connections and their supplying arteries with sacrifice of the diseased venous sinus if it does not contribute to venous drainage of the brain. Management options include endovascular treatment, surgery, or radiotherapy [12]. Of these modalities, endovascular treatment has emerged as the mainstay of management in most cases, except at certain specific anatomical locations such as anterior cranial fossa DAVFs, where surgery offers extremely gratifying results [13–16]. Hybrid procedures have evolved as well, such as direct exposure of the superior ophthalmic vein and venous coiling thereafter. Radiosurgery for intracranial DAVFs offers fistula occlusion rates ranging from 58% to 83% [17,18].
There has been significant evolution in the various endovascular techniques for DAVF treatment. It was in 1979 that Mullan et al. [19] first described embolization of a cavernous sinus DAVF and in 1987 that Hallbach et al. [20] reported the use of transvenous route in order to achieve embolization of a lateral sinus DAVF. Transvenous embolization of the venous sinuses afforded good success rates in the management of these malformations. However, in heavily compartmentalized sinuses or those sinuses which were isolated or sequestered, complete fistula exclusion was not possible. It, however, forms the mainstay of management in locations such as the cavernous sinus. Embolization was earlier performed using transarterially delivered particulates to achieve palliation or combined with other procedures. n-butyl cyanoacrylate has been used using a transarterial approach to treat these fistulae . However, its disadvantages included the need of appropriate glue concentrations, high operator experience, and the high likelihood of incomplete embo-
Sivasankar et al.
27
Journal of Vascular and Interventional Neurology, Vol. 9
Figure 3. (a) Left ECA angiogram lateral projection shows high flow condylar canal DAVF supplied by Ascending pharyngeal artery. (b) Dual tip microcatheter navigated into the venous pouch of the fistula via the transvenous route. However, coils did not achieve satisfactory shape. (c) Microcatheter (arrow) navigated via the Ascending pharyngeal artery close to the point of fistula. (d) Post Squid embolization ECA angiogram lateral projection shows complete exclusion of the fistula. (e) Squid cast seen at the condylar canal (arrow).
lization or catheter entrapment following inappropriate microcatheter position [21]. Further advancements in microcatheter, wire, coil, and EVOH technology have markedly improved the cure rates of this entity, offering a safe and durable result with low complication rates. The use of the liquid embolic agent ethylene vinyl copolymer (EVOH) has greatly improved endovascular management results in intracranial DAVFs. Cognard et al. [21] performed a study of 30 patients of DAVF with cortical venous reflux, who had been treated with Onyx embolization. The cure rate in this group was 80%, and complications occurred in two patients. Similar rates were reported by Saraf et al. [22] in their analysis of 25 cases treated using Onyx. We had similar rates of immediate post-procedural success (81.8%) using EVOH copolymer, which improved to 95% when the cases with slow flow residue on their immediate post-procedural angiograms were followed up. The number of patients treated using transvenous coiling is extremely low in our series and, hence, cannot be used as reliable data for analysis. However, there have been recent reports with regard to the long-term durability of embolization [23].
It has been suggested that the stability of embolization cure rates may be overestimated, as cases of DAVF recanalization have been noted in studies with angiographic follow-up. We could perform six-month control angiograms in nine patients with a special emphasis on including three of the patients who had slow flow residue on their immediate post-operative angiograms. All nine of these patients had stable occlusions. Post-procedural complications related to venous stasis were noted only in two patients, both of which were managed with low molecular weight heparin and made good clinical recovery. A third complication was minor and related to puncture site hematoma which was managed conservatively.
Conclusion Endovascular management of cerebral DAVFs is both efficient and stable with high cure rates and low complication rates. The advancements in microcatheter, microwire, and liquid embolic agent technology have greatly improved management outcomes in this entity. Use of
28
EVOH co-polymer using a transarterial access should form the first line of management in these conditions as it allows for greater injection times, greater penetration, and low complications using a single pedicle. Transvenous coiling is difficult in sinuses which are compartmentalized following venous thrombosis or in isolated sinuses. They, however, form the first line treatment option in locations, such as the cavernous sinus and condylar canal, in order to prevent complications due to uncontrolled spread of liquid embolic agents. Combination of various endovascular modalities may be required as seen in some of our cases, and increase the rate of success achieved.
Journal of Vascular and Interventional Neurology, Vol. 9
References 1. Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 1969;93:1071–1078. 2. Al-Shahi R, et al. Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke 2003;34:1163–1169. 3. Mullan S. Reflections upon the nature and management of intracranial and intraspinal vascular malformations and fistulae. J Neurosurg 1994;80:606–616. 4. Borden JA, et al. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 1995;82:166–179. 5. Cognard C, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 1995;194:671–680. 6. Davies MA, et al. The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 1996;85:830–837. 7. Awad IA, Little JR. Intracranial dural Arterio-venous malformations factors predisposing to an aggressive neurological course. J Neurosurg 1990;72:839–850. 8. Houser OW, et al. Arteriovenous malformation affecting the transverse duralvenous sinus – an acquired lesion. Mayo Clin Proc 1979;54:651–661. 9. Uranishi R, et al. Expression of angiogenic growth factors in dural arteriovenous fi stula. J Neurosurg 1999;91:781–786.
10. Klisch J, et al. Plasma vascular endothelial growth factor and serum soluble angiopoietin receptor sTIE-2 in patients with dural arteriovenous fi stulas: a pilot study. Neuroradiology 2005;47:10– 17. 11. Brown RD Jr, et al. Intracranial dural arteriovenous fi stulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 1994;81:531–538. 12. Kiyosue H, et al. Treatment of intracranial Dural arteriovenous Fistula: Current Strategies based on location and hemodynamics and alternative techniques of transcatheter embolization. Radiographics 2004;24:1637–1651. 13. Giller CA, et al. Multidisciplinary treatment of a large cerebral dural arteriovenous fistula using embolization, surgery and radiosurgery. Proc (BayUniv Med Cent) 2008;21:255–257. 14. Sundt TM Jr, Piepgras DG. The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 1983;59:32–39. 15. Koebbe CJ, et al. Radiosurgery of dural arteriovenous fistulas. Surg Neurol 2005;64:392–399. 16. Lucas CP, et al. Treatment for intracranial dural arteriovenous malformations:a meta-analysis from the English language literature. Neurosurgery 1997;40:1119–1130.discussion 30–32. 17. Koebbe CJ, et al. Radiosurgery for dural arteriovenous fi stulas. Surg Neurol 2005;64:392–398.discussion 8–9. 18. Soderman M, et al. Gamma knife surgery for dural arteriovenous shunts: 25 years of experience. J Neurosurg 2006;104:867–875. 19. Mullan S, Johnson DL. Combined sagittal and lateral sinus dural fistulae occlusion. J Neurosurgery 1995;82:159–165. 20. Halbach VV, et al. Transvenous embolization of dural fistula involving the transverse and sigmoid sinuses. AJNR Am J Neuroradiol 1989;10:385–392. 21. Cognard C, et al. Endovascular treatment of Intracranial dural arteriovenous fistula with cortical venous drainage: New Management using ONYX. AJNR Am J Neuroradiol 2008;29:235–241. 22. Saraf R, et al. Embolization of cranial dural arteriovenous fistulae with ONYX: Indications, techniques, and outcomes. Ind J Radiol Imag 2010;20(1):26–33. 23. Adamczyk P, et al. Recurrence of “cured” dural arteriovenous fistulas after Onyx embolization. Neurosurg Focus 2012;32(5)
2
3
2
2
Rajeev Sivasankar , Raju Augustine George , Rochan Pant , Samresh Sahu , Rohit Aggarwal , and 2 Aftab Alam 1Department 2Dept
of Imaging & interventional Radiology, INHS Asvini, Mumbai 400005
of Radiodiagnosis & Interventional Radiology, Command Hospital Air Force, Bangalore-560007
3Department
of Imaging & interventional Radiology, MH (CTC), Pune, India
Journal of Vascular and Interventional Neurology, Vol. 9
Introduction The true incidence of cerebral dural arteriovenous fistulae (DAVF) is largely unknown [1]. It is estimated that these malformations account for less than 10% of all intracranial vascular malformations [2]. It is hypothesized that these fistulae develop following venous or cortical sinus thrombosis following which multiple fistulous communications develop, typically between numerous branches of the ECA, ICA, and/or vertebral artery and a venous sinus and/or intracranial veins [3]. Any intracranial venous sinus may be involved. Clinical manifestations depend upon the location and anatomy of the lesion. Various classification systems have been used to address the nature of these fistulae; however, the commonly used ones include the Borden classification [4] or the one proposed by Cognard [5]. The aggressive subtypes of DAVFs are associated with retrograde venous sinus, cortical venous, or spinal venous reflux, which lead to intracranial haemorrhage or neurological deficit [6]. Other features suggestive of the aggressiveness of DAVFs are stenosis of the draining sinus, deep venous drainage, certain locations like the anterior cranial fossa and tentorium, venous congestion and venous aneurysm, or varix, mainly in those DAVFs with direct leptomeningeal venous drainage [7]. Endovascular management is now the primary modality of treatment for all DAVFs. We wish to present our experience in treating 22 patients with 25 aggressive intracranial DAVFs using transarterial embolization with ethylene vinyl alcohol (EVOH) co-polymer or transvenous coiling aimed at occlusion of the venous drainage along with all its arterial supply.
Materials and Methods Twenty five aggressive cerebral DAVFs were treated between January 2013 and October 2016 in 22 patients
and data were retrospectively analyzed. Clinical manifestations and locations of 22 patients are shown in Table 1. There were 17 males and 5 females whose age ranged from 30 to 78 years. Five patients had a prior history of treatment for venous sinus thrombosis, one of the patients with multi-focal fistulae had exposure to high altitude for 2 years prior to being symptomatic, and one patient had a prior closed head injury. Four patients had fistulae which had angiographic features conforming to the “benign” variety (Cognard types I and IIa or Borden type I). These were managed conservatively, but patients have been kept under follow-up. All patients underwent angiography and embolization on a single plane angiography unit (Integris, Allura, Philips or Polystar T.O.P, and Siemens). Patients initially underwent a six-vessel cerebral angiogram under local anaesthesia. Patients were chosen for treatment only if angiograms revealed aggressive features (Borden types II or III). Therapeutic embolization was performed in a different session under general anaesthesia using EVOH copolymer in all of the cases except three patients. These included two patients with cavernous sinus DAVFs, which were treated using a transvenous approach and coil embolization, one case of an orbital apex DAVF which was treated using direct superior ophthalmic vein “cut-down” followed by transvenous coiling. This patient had a residual fistula on control angiogram, which was treated using a transarterial approach using EVOH co-polymer. Two of the 22 patients had multifocal fistulae, and the fistulae considered to have the most aggressive features were targeted first. The usual approach for transarterial embolization involved using a 6F common femoral arterial access and placement of a 6F guiding catheter (Envoy, Codman Neurovascular or Guider, Stryker Neurovascular) in the ECA or the verte-
Vol. 9, No. 4, pp. 22–28. Published June, 2017. All Rights Reserved by JVIN. Unauthorized reproduction of this article is prohibited Corresponding Author: Rajeev Sivasankar MD DNB FINR, Sr Adv (Rad) and Interventional Neuroradiologist, Department of Imaging and Interventional Radiology, INHS Asvini, Mumbai, India.
Sivasankar et al.
23
Table 1. S. No Location 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
Journal of Vascular and Interventional Neurology, Vol. 9
15. 16. 17. 18. 19. 20. 21. 22.
Lateral sinus Lateral sinus Orbital apex Tentorial Lateral sinus Condylar canal Mastoid emissary Lateral sinus Cavernous sinus Jugular bulb SSS Lateral sinus Cavernous sinus Parietal Cortical vein (type III) Jugular bulb Lateral sinus Cortical vein (Borden III) + Jugular bulb+ Lateral sinus Lateral sinus + Jugular bulb Tentorial Cavernous sinus Torcular & Medial transverse Lateral sinus
Headaches Visual symptoms + + + + + + + + + + + + -
Papilledema Seizures ICH Tinnitus Cognitive impairment + + + + + + + + + + + + + + + + + + + +
Neurological deficits + + + + + -
+
+
+
-
-
+ + -
+
-
+ + + -
+ -
-
-
-
+ +
+ -
+ -
bral artery. A dimethyl sulfoxide (DMSO) compatible flow guided microcatheter (Marathon or Apollo, Medtronic) was used in all cases over 0.008” microwire (Mirage, Covidien/Medtronic) or 0.012” microwire (Traxcess, Microvention) to access the artery and navigate as close to the fistulous site as possible). After suitability of microcatheter position was ascertained using microcatheter angiograms, the microcatheters were flushed using 10 cc of saline and dead space filled with 0.3 cc of DMSO. Thereafter, tantalum admixed EVOH co-polymer (Onyx, EV3/Medtronic or Squid, Emboflu) was injected using the standard “plug and push” method so as to achieve exclusion of fistulae. Sixteen out of 25 fistulae were embolized using Squid-12, while seven (including the repeat embolization for the residual orbital apex DAVF) were embolized using Onyx-18. In none of the cases, other concentrations of Squid or Onyx used. Endovascular technique for transvenous coiling involved placing a 6F guiding catheter (Envoy, Codman Neurovascular or Guider, Stryker Neurovascular) in the IJV and a 4F diagnostic H1 catheter in the ICA. A dual tip microcatheter (Echelon-10, EV3) was navigated over a 0.014” microwire (Synchro-14, Stryker Neurovascular or Traxcess-14, Microvention) via the inferior petrosal sinus to reach the cavernous sinus and further into the superior ophthalmic vein. Thereafter, multiple detachable platinum microcoils were used to achieve exclusion of the fistula. All patients were extubated postoperatively. Two patients were on short-term anticoagulation for 24 hours for post-procedural venous stasis. Patients were followed up clinically at one month, with MRI at three months and a control cerebral angiogram performed when possible at 6 months. All patients under-
went post-operative CT scans to exclude haemorrhagic procedural complications.
Results Location Based on location, nine of the 25 DAVFs (36%) occurred at the lateral sinus (transverse-sigmoid sinus), four at the jugular bulb (16%), three occurred at the cavernous sinus (12%), two each were at the cortical veins, tentorial sinus (8% each), one each occurred at the orbital apex, mastoid emissary, condylar canal, SSS, and torcula (4% each). Clinical presentation Twelve of 22 patients had headaches (54.5%), 11 had tinnitus (50%), 8 of 22 (36.3%) had cognitive impairment on mini-mental status examination, 6 of 22 (27.3%) had neurological deficits, 6 of 22 (27.3%) had visual symptoms (chemosis, proptosis, and/or exophthalmos), 5 had papilledema (22.8%), and 3 had intra cerebral haemorrhage (13.6%). In patients with lateral sinus DAVFs, four of nine (44.5%) patients had headaches and seven of nine (77.8%) had tinnitus. Those with cavernous sinus DAVFs presented with visual symptoms (3/3, 100%), neurological deficits (cranial nerve palsies in 2/3, 66.7%), or papilledema (2/3, 66.7%). Endovascular treatment results Twenty two patients in this study group had 25 fistulae embolized. In the group in which EVOH was used, of the 22 fistulae, complete occlusion on immediate post-
24
Journal of Vascular and Interventional Neurology, Vol. 9
procedural angiogram was achieved in 18 ( 81.8%) of the fistulae. Three of the fistulae had marked slow flow on immediate post-procedural angiograms (13.6%), which, however, were completely occluded on their control angiograms. Six-month control angiograms were performed in nine patients, which showed stable occlusions. One patient with multi-focal DAVFs had partial embolization of his lateral sinus fistula, which required another session of treatment using an alternate arterial pedicle (4.5%). Of the three patients who underwent transvenous coiling, two of the patients with cavernous sinus DAVFs achieved good post-procedural result (66.6%). The patient with an orbital apex DAVF, which required direct superior ophthalmic vein access and transvenous coiling, showed an initial good angiographic result but had a residual fistula on follow-up angiogram. This was treated by the transarterial route using the accessory meningeal artery. A total of 27 arteries were embolized: the middle meningeal artery in 21, the occipital artery in 2, accessory meningeal artery in 1, the ascending pharyngeal in 2, and the posterior meningeal artery in 1. The volume of EVOH injected ranged from 0.3 cc to 8 cc per procedure. The duration of injection per pedicle ranged from 20 min to 60 min. In the overall analysis of the endovascular treatment experience, all fistulae (25/25) achieved angiographic exclusion at the end of their treatment sessions. Complications Two patients developed post embolization headaches and drowsiness, which was probably due to venous stasis. This was managed with anticoagulation and recovery was uneventful. Another patient had a groin hematoma which was managed conservatively. Representative cases Case 1—A 62-year-old male presented with history of headaches and gradually progressive weakness of both upper and lower limbs since one year. On examination, patient had neurocognitive decline on mini-mental status examination, reduced power (grade III/V in both upper limbs and II/V both lower limbs). His MRI revealed prominent and dilated veins in both cerebral hemispheres and around the brain stem. Cerebral angiogram [Figure 1(a)] revealed aggressive high flow dural fistulae involving his right lateral sinus (single arrow) and jugular bulb (double arrow) with reflux into his venous sinuses and deep veins [Figure 1(b)]. Reflux into the spinal perimedullary venous system accounted for his limb weakness. Marked cortical venous congestion [Figure 1(c)] was present in both cerebral hemispheres.
The right lateral sinus high flow dural AVF was treated in the first session using transarterial approach via the middle meningeal artery and injection of Onyx-18. Post embolization angiogram revealed a small residual fistula present in the medial aspect of the right transverse sinus [Figure 1(d)] and high flow right jugular bulb fistula [Figure 1(e)]. The jugular bulb fistula was treated using via the Ascending pharyngeal artery and Onyx injection. Complete exclusion of fistula was achieved [Figure 1(f)–(h)]. Thereafter, the residual fistula in the medial aspect of the transverse sinus DAVF was treated using the posterior meningeal artery and embolization done using Onyx-18 [Figure 1(i)–(l)]. Complete exclusion of the fistulae was obtained and the patient made a full recovery. Case 2—Seventy-two-year-old man with a past history of head injury 25 years ago presented with progressively increasing swelling behind his left ear since seven years, which were associated with headaches. Examination revealed a pulsatile, soft swelling over his mastoid region. There was history of having been taken up for embolization at some other centre five years ago, and fistula partially embolized. Cerebral angiogram [Figure 2(a)] revealed a high flow mastoid emissary fistula supplied by branches of the middle meningeal artery and occipital artery (single arrow). There were marked cortical venous reflux and presence of venous aneurysms (double arrows). Transarterial approach was used via the middle meningeal artery [Figure 2(b)] and fistula embolized using Squid-12. Post embolization angiogram revealed complete exclusion of the fistula [Figure 2(c) and (d)]. Case 3—Sixty-five-year-old lady presented with headaches, bilateral chemosis, and proptosis for 4 months. MRI revealed a small old right temporal bleed. Cerebral angiogram showed a high flow left condylar canal dural AVF with extensive reflux into both hemispheres [Figure 3(a)]. Patient was taken for endovascular treatment via the transvenous route [Figure 3(b)]; however, platinum microcoils would not take the desired shape of the pouch and a transarterial route via the ascending pharyngeal artery used with Squid embolization [Figure 3(c)]. Post-embolization angiogram shows exclusion of the fistula with EVOH cast at the condylar canal [Figure 3(d) and (e)].
Discussion Cerebral DAVFs are uncommon lesions which account for about 10% of intracranial vascular malformations [2]. These fistulae occur as direct connections between
Sivasankar et al.
25
Journal of Vascular and Interventional Neurology, Vol. 9
Figure 1. Multi-focal DAVFs. (a) Right ECA angiogram AP projection shows high flow DAVF at the right lateral sinus
(single arrow) and another at the right jugular bulb (double arrow). the sinus is occluded. (b) Right ECA angiogram lateral projection demonstrates the marked reflux into venous sinuses and deep veins. (c) There was associated reflux into the spinal perimedullary venous system which accounted for his limb weakness. Marked cortical venous congestion was present in both cerebral hemispheres. (d) Post embolization right CCA angiogram Towne projection shows jugular bulb fistula (single arrow) and residual right transverse sinus fistula with Onyx cast (double arrow) occupying most of the right transverse sinus. (e) Right CCA angiogram lateral projection shows the jugular bulb fistula (arrow) supplied by the Neuromeningeal trunk. (f) Marathon microcatheter (arrow) navigated into the Neuromeningeal trunk and a 4 mm x 15 mm compliant balloon placed in the ipsilateral vertebral artery for protection (double arrows). Onyx cast (white star) is seen in the right transverse sinus from the first session of embolization. (g) Post embolization ECA angiogram shows complete exclusion of jugular bulb DAVF with residual fistula at the lateral sinus fed by branches of the occipital artery. (h) Onyx cast seen in the right transverse sinus (single arrow) and right jugular bulb (double arrows) at the end of the second session of embolization. (i) and (j) Right VA angiograms in Towne and lateral projections show supply to the right transverse sinus fistula from posterior meningeal artery (arrow). (k) Microcatheter navigated into the posterior meningeal artery. (l) Post embolization right VA angiogram shows complete exclusion of the lateral sinus fistula.
one or more arteries that supply the dura mater and are usually acquired conditions. Current evidence favors their occurrence as explained by the three stage hypothesis, wherein the initial event is that of venous sinus thrombosis, following which nascent fistulae develop on the walls of the sinus between the dural arteries and the venous tributaries as a result of the action of various
angiogenetic and inflammatory factors. These fistulous connections enlarge over time and attempt to recanalize the sinus. The presence of increased venous back pressure, stenosis, or occlusion results in reflux of the now arterialized blood into other sinuses or leptomeningeal veins [8–10].
26
Journal of Vascular and Interventional Neurology, Vol. 9
Figure 2. (a) Mastoid emissary DAVF. Single arrow: point of fistula supplied by branches of the MMA and occipital artery. Double arrow: venous aneurysms and the marked cortical venous reflux. (b) Mastoid emissary DAVF. Single arrow: microcatheter navigated close to the fistulous point. (c) and (d) Squid used as embolic agent. Post embolization ECA angiogram lateral projection shows complete exclusion of fistula.
There is a direct correlation between the degree of venous reflux and the incidence of cerebral haemorrhage, which mandates early management of aggressive cerebral dural AVFs [4,5]. The overall annual risk of haemorrhage in patients with intracranial dAVFs is 1.8%, with a case fatality rate of 20% with haemorrhage [11]. The aim of management is to occlude the fistulous connections and their supplying arteries with sacrifice of the diseased venous sinus if it does not contribute to venous drainage of the brain. Management options include endovascular treatment, surgery, or radiotherapy [12]. Of these modalities, endovascular treatment has emerged as the mainstay of management in most cases, except at certain specific anatomical locations such as anterior cranial fossa DAVFs, where surgery offers extremely gratifying results [13–16]. Hybrid procedures have evolved as well, such as direct exposure of the superior ophthalmic vein and venous coiling thereafter. Radiosurgery for intracranial DAVFs offers fistula occlusion rates ranging from 58% to 83% [17,18].
There has been significant evolution in the various endovascular techniques for DAVF treatment. It was in 1979 that Mullan et al. [19] first described embolization of a cavernous sinus DAVF and in 1987 that Hallbach et al. [20] reported the use of transvenous route in order to achieve embolization of a lateral sinus DAVF. Transvenous embolization of the venous sinuses afforded good success rates in the management of these malformations. However, in heavily compartmentalized sinuses or those sinuses which were isolated or sequestered, complete fistula exclusion was not possible. It, however, forms the mainstay of management in locations such as the cavernous sinus. Embolization was earlier performed using transarterially delivered particulates to achieve palliation or combined with other procedures. n-butyl cyanoacrylate has been used using a transarterial approach to treat these fistulae . However, its disadvantages included the need of appropriate glue concentrations, high operator experience, and the high likelihood of incomplete embo-
Sivasankar et al.
27
Journal of Vascular and Interventional Neurology, Vol. 9
Figure 3. (a) Left ECA angiogram lateral projection shows high flow condylar canal DAVF supplied by Ascending pharyngeal artery. (b) Dual tip microcatheter navigated into the venous pouch of the fistula via the transvenous route. However, coils did not achieve satisfactory shape. (c) Microcatheter (arrow) navigated via the Ascending pharyngeal artery close to the point of fistula. (d) Post Squid embolization ECA angiogram lateral projection shows complete exclusion of the fistula. (e) Squid cast seen at the condylar canal (arrow).
lization or catheter entrapment following inappropriate microcatheter position [21]. Further advancements in microcatheter, wire, coil, and EVOH technology have markedly improved the cure rates of this entity, offering a safe and durable result with low complication rates. The use of the liquid embolic agent ethylene vinyl copolymer (EVOH) has greatly improved endovascular management results in intracranial DAVFs. Cognard et al. [21] performed a study of 30 patients of DAVF with cortical venous reflux, who had been treated with Onyx embolization. The cure rate in this group was 80%, and complications occurred in two patients. Similar rates were reported by Saraf et al. [22] in their analysis of 25 cases treated using Onyx. We had similar rates of immediate post-procedural success (81.8%) using EVOH copolymer, which improved to 95% when the cases with slow flow residue on their immediate post-procedural angiograms were followed up. The number of patients treated using transvenous coiling is extremely low in our series and, hence, cannot be used as reliable data for analysis. However, there have been recent reports with regard to the long-term durability of embolization [23].
It has been suggested that the stability of embolization cure rates may be overestimated, as cases of DAVF recanalization have been noted in studies with angiographic follow-up. We could perform six-month control angiograms in nine patients with a special emphasis on including three of the patients who had slow flow residue on their immediate post-operative angiograms. All nine of these patients had stable occlusions. Post-procedural complications related to venous stasis were noted only in two patients, both of which were managed with low molecular weight heparin and made good clinical recovery. A third complication was minor and related to puncture site hematoma which was managed conservatively.
Conclusion Endovascular management of cerebral DAVFs is both efficient and stable with high cure rates and low complication rates. The advancements in microcatheter, microwire, and liquid embolic agent technology have greatly improved management outcomes in this entity. Use of
28
EVOH co-polymer using a transarterial access should form the first line of management in these conditions as it allows for greater injection times, greater penetration, and low complications using a single pedicle. Transvenous coiling is difficult in sinuses which are compartmentalized following venous thrombosis or in isolated sinuses. They, however, form the first line treatment option in locations, such as the cavernous sinus and condylar canal, in order to prevent complications due to uncontrolled spread of liquid embolic agents. Combination of various endovascular modalities may be required as seen in some of our cases, and increase the rate of success achieved.
Journal of Vascular and Interventional Neurology, Vol. 9
References 1. Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 1969;93:1071–1078. 2. Al-Shahi R, et al. Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke 2003;34:1163–1169. 3. Mullan S. Reflections upon the nature and management of intracranial and intraspinal vascular malformations and fistulae. J Neurosurg 1994;80:606–616. 4. Borden JA, et al. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 1995;82:166–179. 5. Cognard C, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 1995;194:671–680. 6. Davies MA, et al. The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 1996;85:830–837. 7. Awad IA, Little JR. Intracranial dural Arterio-venous malformations factors predisposing to an aggressive neurological course. J Neurosurg 1990;72:839–850. 8. Houser OW, et al. Arteriovenous malformation affecting the transverse duralvenous sinus – an acquired lesion. Mayo Clin Proc 1979;54:651–661. 9. Uranishi R, et al. Expression of angiogenic growth factors in dural arteriovenous fi stula. J Neurosurg 1999;91:781–786.
10. Klisch J, et al. Plasma vascular endothelial growth factor and serum soluble angiopoietin receptor sTIE-2 in patients with dural arteriovenous fi stulas: a pilot study. Neuroradiology 2005;47:10– 17. 11. Brown RD Jr, et al. Intracranial dural arteriovenous fi stulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 1994;81:531–538. 12. Kiyosue H, et al. Treatment of intracranial Dural arteriovenous Fistula: Current Strategies based on location and hemodynamics and alternative techniques of transcatheter embolization. Radiographics 2004;24:1637–1651. 13. Giller CA, et al. Multidisciplinary treatment of a large cerebral dural arteriovenous fistula using embolization, surgery and radiosurgery. Proc (BayUniv Med Cent) 2008;21:255–257. 14. Sundt TM Jr, Piepgras DG. The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 1983;59:32–39. 15. Koebbe CJ, et al. Radiosurgery of dural arteriovenous fistulas. Surg Neurol 2005;64:392–399. 16. Lucas CP, et al. Treatment for intracranial dural arteriovenous malformations:a meta-analysis from the English language literature. Neurosurgery 1997;40:1119–1130.discussion 30–32. 17. Koebbe CJ, et al. Radiosurgery for dural arteriovenous fi stulas. Surg Neurol 2005;64:392–398.discussion 8–9. 18. Soderman M, et al. Gamma knife surgery for dural arteriovenous shunts: 25 years of experience. J Neurosurg 2006;104:867–875. 19. Mullan S, Johnson DL. Combined sagittal and lateral sinus dural fistulae occlusion. J Neurosurgery 1995;82:159–165. 20. Halbach VV, et al. Transvenous embolization of dural fistula involving the transverse and sigmoid sinuses. AJNR Am J Neuroradiol 1989;10:385–392. 21. Cognard C, et al. Endovascular treatment of Intracranial dural arteriovenous fistula with cortical venous drainage: New Management using ONYX. AJNR Am J Neuroradiol 2008;29:235–241. 22. Saraf R, et al. Embolization of cranial dural arteriovenous fistulae with ONYX: Indications, techniques, and outcomes. Ind J Radiol Imag 2010;20(1):26–33. 23. Adamczyk P, et al. Recurrence of “cured” dural arteriovenous fistulas after Onyx embolization. Neurosurg Focus 2012;32(5)
