Transvenous Embolization of Cavernous Sinus Dural Arteriovenous Fistulas with Shunts Involving the Laterocavernous Sinus

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1 Journal of Neuroendovascular Therapy 2017; 11: 1 7 Online November 9, 2016 DOI: /jnet.oa Transvenous Embolization of Cavernous Sinus Dural Arteriovenous Fistulas with Shunts Involving the Laterocavernous Sinus Mika Okahara, 1,2 Hiro Kiyosue, 2 Yuzo Hori, 3 Satomi Ide, 3 Syuichi Tanoue, 2 and Hiromu Mori 2 Purpose: The laterocavernous sinus (LCS) is a normal variation of the venous sinus bordered by the dura mater lateral to the cavernous sinus (CS) and one of the major drainage route of the superficial middle cerebral vein (SMCV). In this study, we evaluated the angiographic findings and the procedure and results of transvenous embolization (TVE) in patients with a cavernous sinus dural arteriovenous fistula (CSDAVF) involving the LCS, and discussed technical tips and pit fall in treatment. In 27 patients with a CSDAVF who underwent TVE between January 2007 and October 2015, we evaluated their three-dimensional digital subtraction angiography/digital angiography (3D-DSA/DA) and selective arteriography about the presence or absence of a shunt to the LCS. Subsequently, in patients with a shunt to the LCS, the angiographic findings and the procedure and results of TVE were evaluated. Results: A shunt to the LCS was observed in four patients (14.8%). In all the four patients, there were multiple shunted pouches of the CS and LCS, and the feeders to the LCS were the artery of the foramen rotundum, middle meningeal artery, and accessory meningeal artery. Reflux to the SMCV and/or uncal vein (UV) via the LCS was present in all the patients. The LCS was connected to the CS at a dorsal site in two patients and at a lateral site in two patients. In all the patients, embolization was performed by advancing a microcatheter to the LCS, but insertion into the LCS was timeconsuming in the patients with CS-LCS connection at a dorsal site. The symptoms disappeared without complications in all the patients. Conclusion: Microcatheter insertion into the LCS is sometimes difficult in patients with CS-LCS connection at a dorsal site, requiring careful attention. In patients with a shunt to the LCS, since embolization of the CS alone can result in Borden type 3 in which cortical venous reflux remains, it is necessary to be careful. Keywords dural arteriovenous fistula, cavernous sinus, laterocavernous sinus Introduction The usefulness of endovascular treatment for dural arteriovenous fistulas has already been established. Transvenous embolization (TVE) has been used as a standard 1 Department of Radiology, Shinbeppu Hospital, Beppu, Oita, Japan 2 Faculty of Medicine, Department of Radiology, Oita University, Yufu, Oita, Japan 3 Department of Radiology, Nagatomi Neurosurgical Hospital, Oita, Oita, Japan Received: May 6, 2016; Accepted: August 23, 2016 Corresponding author: Mika Okahara. Department of Radiology, Shinbeppu Hospital, 3898 Tsurumi, Beppu, Oita , Japan okahara@oita-u.ac.jp 2016 The Editorial Committee of Journal of Neuroendovascular Therapy. All rights reserved. treatment for cavernous sinus dural arteriovenous fistulas (CSDAVFs), which successfully obliterate the CSDAVFs in the majority of cases without complication. 1,2) The laterocavernous sinus (LCS) is located lateral to the lateral component of the cavernous sinus (CS), and is a normal variation of a sinus that is separated from CS by the inner dural layer and one of the major drainage pathways of the superficial middle cerebral vein (SMCV). The LCS drains into the posterior aspect of the CS, or penetrates the middle cranial fossa, draining into the pteygoid plexus, or runs dorsally, draining into the transverse sinus. 3,4) In some patients with a CSDAVF, a shunt to the LCS is present, or the LCS is a drainage pathway. 5 7) In this study, we evaluated the angiographic findings and the TVE procedure and results in CSDAVF patients with a shunt to the LCS, and discussed the cautionary points in treatment. 1

2 Okahara M, et al. Table 1 Characteristics of four patients of cavernous sinus dural arteriovenous fistulas with shunts involving the laterocavernous sinus Patient no. Age/sex Symptoms Site Borden s type IPS 1 72/F Diplopia, chemosis, tinnitus Right II Occluded 2 61/F Diplopia, chemosis, tinnitus Left II Patent 3 64/F Diplopia, chemosis Right II Occluded 4 75/F Chemosis Right II Occluded IPS: inferior petrosal sinus Materials and Methods Between January 2007 and October 2015, 27 patients were treated by TVE for a CSDAVF, of whom four (14.8%) showed a shunt to the LCS. In these four patients, preoperative angiographic findings and the treatment procedure were retrospectively evaluated. All the four patients were females and the patients ages ranged years (mean: 68 years). All the patients were classified as Borden type 2 dural arteriovenous fistulas. The inferior petrosal sinus (IPS) on the affected side was occluded in three patients. As the chief complaint, eye symptoms were observed in all the patients and were accompanied by tinnitus in two patients. The clinical characteristics of the patients are shown in Table 1. Selective digital subtraction angiography (DSA) of the bilateral internal carotid arteries, external carotid arteries, and vertebral arteries was performed using a biplane angiography system (Innova 3131, GE Medical Systems, Milwaukee; Infinix VB, Toshiba Medical, Tokyo) in all the patients. When CSDAVFs were found using conventional DSA, three-dimensional (3D) rotational angiography was subsequently performed. 3D images with maximum intensity projection (MIP), volume rendering reconstruction (VR) as well as multiplanar reconstruction (MPR) images composed of slices with mm thickness and a 0.5 mm interval were obtained from data of rotational angiography using workstation (Advanced Workstation, GE Healthcare Milwaukee; Ziostation, Zio, Tokyo). All angiographic images were reviewed by two experienced neuroradiologists with over 10 years of experience in interventional neuroradiology, who reached a consensus regarding the shunted pouches, feeding arteries, the site of the shunt to the LCS, drainage route, the pattern of connection between CS and LCS, and the drainage patterns of the SMCV and uncal vein (UV). TVE was performed under local anesthesia in all the patients. In four patients with a shunt to the LCS, the approach route was the ipsilateral IPS, ipsilateral occluded IPS, contralateral IPS via the intercavernous sinus, and ipsilateral obstructed IPS and basilar plexus, respectively. Follow-up angiography was performed 1 week after embolization. When there is no residual shunt, MR angiography was performed after 3 months and subsequently at 6-month intervals for follow-up observation. The relationship between the CS-LCS connection pattern and the degree of difficulty in microcatheter advancement, treatment results immediately after TVE and at follow-up, and complications, were also evaluated. Results Table 2 shows the angiographic findings in four patients (14.8%) with a shunt to the LCS among the 27 patients who underwent TVE for CSDAVF. In addition to a shunted pouch in the LCS, shunted pouches in the CS were observed in all the four patients, including three patients with multiple shunted pouches. In one patient, there was also a shunted pouch in the sphenoparietal sinus. The feeding arteries to the shunted pouch of the LCS were the middle meningeal artery (n = 2), artery of the foramen rotundum (n = 3), and accessory meningeal artery (n = 2). In the report about the anatomical variation in termination of the UV, the variations of junction between the UV and/or SMCV and LCS were also described. 8) In this study, the UV joined the SMCV, before joining the LCS in three patients. In the other patient (case 3), the UV alone joined the LCS in the absence of SMCV involvement in the LCS. The shunt to the LCS was located at a posterior site of the LCS in three patients and anterior aspect to the UV-LCS junction site in one patient (case 3) (Fig. 1). In the drainage route, reflux to the superior ophthalmic vein was observed in all the patients, reflux from the LCS to the SMCV and UV in three patients, and reflux from the LCS to UV in one patient (case 3) in whom the UV alone joined the LCS. In addition, reflux to the prepontine bridging vein was present in two patients and drainage to the contralateral side via the intercavernous sinus in two patients. 2

3 Transvenous Embolization of CSDAVFs Table 2 Angiographical features of patients Patient no. Shunted pouch Feeding arteries Shunted site of LCS Connection site between CS and LCS Drainage route 1 LCS MMA, AFR Posterior site of LCS Dorsal LCS-SMCV-UV CS Prepontine bridging vein Posteromedial APA SPS, SOV Medial APA, AFR Sphenoparietal sinus MMA, AFR, AMA 2 LCS MMA, AMA Posterior site of LCS Lateral LCS-SMCV-UV CS Prepontine bridging vein Posteromedial APA SOV Posterolateral AFR, MMA ICS-contralateral Lateral MMA, AFR, AMA SOV/IPS 3 LCS AFR Anterior site of junction of UV and LCS Dorsal LCS-UV CS SOV Anterolateral MMA, AFR, AMA Posterolateral RMA from OPA 4 LCS AMA, AFR Posterior site of LCS Lateral LCS-SMCV-UV CS SOV Medial AMA, APA ICS-contralateral Posterolateral MMA, AMA, APA SOV Posteromedial MMA, AMA, APA AFA: artery of foramen rotundum; AMA: accessory meningeal artery; APA: ascending pharyngeal artery; CS: cavernous sinus; ICS: intercavernous sinus; IPS: inferior petrosal sinus; LCS: laterocavernous sinus; MMA: middle meningeal artery; OPA: ophthalmic artery; RMA: recurrent meningeal artery; SMCV: superior middle cerebral vein; SOV: superior ophthalmic vein; SPS: superior petrosal sinus; UV: uncal vein 3

4 Okahara M, et al. (a) (b) (c) (d) Fig. 1 Case 3: A 64-year-old female presenting with right chemosis and diplopia. Sagittal partial MIP image of rotational angiography of right external carotid angiography (a) shows the dural arteriovenous fistula involving the right CS and LCS draining into the superior ophthalmic vein and UV. Shunt to LCS (arrows) is present to the anterior aspect of LCS connecting with UV, and the LCS connects to the posterior aspect of CS. Lateral view (b) of selective venography after coil embolization of an anterolateral shunted pouch of CS shows the microcatheter tip located in the LCS. UV is also noted. Lateral view of right maxillary angiography (c) after coil embolization of LCS shows the residual shunt of LCS and reflux for deep venous system through the UV. Lateral view of right maxillary angiography (d) after 33% NBCA-LPD injection from LCS and coil embolization of a posterolateral shunted pouch of CS shows the disappearance of the cavernous sinus dural arteriovenous fistula. CS: cavernous sinus; LCS: laterocavernous sinus; MIP: maximum intensity projection; NBCA-LPD: n-butyl cyanoacrylate lipiodol; UV: uncal vein The approach route was the ipsilateral IPS (occluded in one patient) in two patients, contralateral IPS via the intercavernous sinus in one patient, and the ipsilateral occluded IPS and basilar plexus in one patient. The treatment procedure, treatment results, and the recurrence in follow-up period are shown in Table 3. CS-LCS junction was present at a dorsal site in two patients and at a lateral site in two patients (Case 4, Fig. 2). In the former, microcatheter insertion from the CS to the LCS was difficult and time-consuming (Case 3, Fig. 1). After the first treatment, the shunt disappeared in three patients. In the other patient, the cortical venous reflux disappeared but the shunt to the CS remained after the first treatment, 4 and the shunt completely disappeared after the third treatment. Neither definite complications nor recurrence during the follow-up period was observed. Discussion The LCS is derived from the primitive tentorial sinus that drains cortical blood from the SMCV. This sinus forms when the primitive tentorial sinus migrates medially toward the CS region at the time of the formation of the lateral wall of the CS during the 8th week of gestation.3) San Millán Ruíz et al.,4) who evaluated 58 sides of 29 autopsy cases, observed the LCS in 14 sides (24.1%), observed that the

5 Transvenous Embolization of CSDAVFs Table 3 Procedure, treatment result, complications, and follow-up Recurrence/follow-up period Treatment results Difficulty of insertion of microcatheter into LCS Connection site between CS and LCS Patient no. Approach route None/103 months 1 Ipsilateral patent IPS Dorsal Difficult Marked regression (Complete occlusion at third procedure) Lateral Easy Complete occlusion None/101 months 2 Ipsilateral occluded IPS 3 Contralateral IPS-ICS Dorsal Difficult Complete occlusion None/13 months Lateral Easy Complete occlusion None/8 months 4 Ipsilateral occluded IPS basilar plexus CS: cavernous sinus; ICS: intercavernous sinus; IPS: inferior petrosal sinus; LCS: laterocavernous sinus SMCV was in continuation with the LCS in 13 sides, and the UV alone was in continuation with the LCS in the absence of SMCV involvement in the LCS in the other. In this study, the UV joined the SMCV before joining the LCS in three patients, whereas the UV alone was connected to the anterior aspect of the LCS in the absence of continuation between the SMCV and LCS in one patient (Fig. 1). There were two patterns of connection between the LCS and CS. One was the termination of the LCS into the posterior aspect of the CS (Fig. 1), and the other was connection between the LCS and the medial layer of the lateral wall of the CS in the portion where the LCS, which was in continuation with the pterygoid plexus or superior petrosal sinus, runs close to the CS. (Fig. 2). 3,4) Gailloud et al., 3) who evaluated the LCS based on angiographic findings, observed an LCS in 22% (22/100), and confirmed that the LCS was in continuation with the CS in 36.5% (8/22), terminating into the dorsal aspect of the CS in 32% (7/22). The laterosellar blood spaces should be divided into two independent system; a medial system includes the superior ophthalmic vein, CS, and IPS; and a lateral system draining the cortical blood of the cerebral convexity through the SMCV toward the pterygoid plexus and/or the transverse sinus. The latter pathway may take the form of a paracavernous sinus, LCS, or a classic termination of the SMCV into the anterior superior aspect of CS. The CSDAVF patients with cortical venous reflux to this lateral system are classified as Borden type 2 or higher grades with reflux to the cortical or deep veins and have a high risk of bleeding. Lv et al. 5,6) have reported about the endovascular treatment for CSDAVFs accompanied by venous drainage to the LCS, and observed reflux into the SMCV or petrosal vein via the LCS in 7 (21.8%) of 32 CSDAVF patients. 6) They reported complete cure without complications after TVE in three patients and transarterial embolization in the other four patients. San Millán Ruíz et al. 7) performed transarterial embolization in patients with a CSDAVF accompanied by cortical venous reflux, but observed aggravation of headache after the procedure, and confirmed by angiogram that cortical venous reflux remained. Since DSA showed a shunt in the LCS draining into the pterygoid plexus without connection with the CS, they advanced a microcatheter from the pterygoid plexus to the LCS, performed TVE, and achieved complete occlusion. Thus, in TVE when not only the LCS is a drainage pathway, but also there is a shunt in the LCS, embolization of the CS alone, leaving the shunt to the LCS has a high risk of Borden type 3 with retrograde cortical venous drainage 5

6 Okahara M, et al. (a) (b) (c) (d) Fig. 2 Case 4: A 75-year-old female presenting with right chemosis. Sagittal MIP image of rotational angiography of right external carotid angiography (a) shows the dural arteriovenous fistula involving the right CS and LCS draining into the superior ophthalmic vein, SMCV, and UV. And the shunt to LCS is also shown (white arrow). The axial reformatted image (b) of the right external carotid angiography shows the shunted pouches of the right CS. And the connection between the CS and LCS is shown (white arrowhead). Front-caudal view (c) shows the shunt of a CS and LCS (arrow), and also shows the drainage to the SOV, SMCV, DMCV, and basal vein. Lateral view (d) of right common carotid angiography after shunted pouches of a CS and LCS shows the disappearance of the CS dural arteriovenous fistula. CS: cavernous sinus; DMCV: deep middle cerebral vein; LCS: laterocavernous sinus; MIP: maximum intensity projection; SMCV: superior middle cerebral vein; SOV: superior ophthalmic vein; UV: uncal vein alone. It is necessary that the microcatheter insertion into the LCS and embolization of LCS. In our study, a shunt to the LCS was observed in 4 (14.8%) of 27 CSDAVF patients, and connection between the LCS and CS was present at a posterior site in two patients and a lateral site in two patients. In patients in whom the LCS connects to a posterior site of the CS, microcatheter insertion into the LCS was time-consuming because the microcatheter inserted from a site anterior to the CS should be once inverted on the dorsal side and inserted into the LCS. It is necessary to confirm the site of connection between the CS and LCS before treatment. However, the adequate understanding of the CS-LCS relationship is difficult using conventional DSA alone, and observation of MPR images using rotational angiography is useful. Conclusion In patients with a shunt to the LCS, since embolization of the CS alone can result in Borden type 3 with retrograde cortical venous drainage alone, it is necessary to be careful. Microcatheter insertion into the LCS is sometimes difficult in patients with CS-LCS connection at a dorsal site; therefore, we should adequately evaluate the angioarchitecture of CSDAVF before procedure. 6

7 Transvenous Embolization of CSDAVFs Disclosure Statement The first author and co-authors have no conflicts of interest. References 1) Kirsch M, Henkes H, Liebig T, et al: Endovascular management of dural carotid-cavernous sinus fistulas in 141 patients. Neuroradiology 2006; 48: ) Kiyosue H, Hori Y, Okahara M, et al: Treatment of intracranial dural arteriovenous fistulas: current strategies based on location and hemodynamics, and alternative techniques of transcatheter embolization. Radiographics 2004; 24: ) Gailloud P, San Millán Ruíz D, Muster M, et al: Angiographic anatomy of the laterocavernous sinus. AJNR Am J Neuroradiol 2000; 21: ) San Millán Ruíz D, Gailloud P, de Miquel Miquel MA, et al: Laterocavernous sinus. Anat Rec 1999; 254: ) Lv X, Jiang C, Li Y, et al: The laterocavernous sinus system: venous inflows, venous outflows, and clinical significance. World Neurosurg 2011; 75: 90 93; discussion ) Lv X, Jiang C, Li Y, et al: Endovascular treatment of dural fistulas with the venous outflow of laterocavernous sinus. Eur J Radiol 2010; 75: e129 e134. 7) San Millán Ruíz D, Oka M, Fasel JH, et al: Transvenous embolization of a dural arteriovenous fistula of the laterocavernous sinus through the pterygoid plexus. Neuroradiology 2007; 49: ) Ide S, Kiyosue H, Tanoue S, et al: Anatomical variations in termination of the uncal vein and its clinical implications in cavernous sinus dural arteriovenous fistulas. Neuroradiology 2014; 56: