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Show Stereotactic Radiosurgery in the Treatment of a Dural Carotid-Cavernous Fistula Gabriel T. Chong, MD, Srinivasan Mukundan, MD, John P. Kirkpatrick, MD, PhD, Ali Zomorodi, MD, John H. Sampson, MD, PhD, M. Tariq Bhatti, MD Abstract: Because of the success of stereotactic radio-surgery (SRS) in the treatment of cerebral arteriovenous malformations (AVMs), SRS is being applied to the treatment of carotid-cavernous dural arteriovenous fistu-las (CCDAVFs) when these lesions are not accessible endovascularly. We report a patient with a CCDAVF that could not be accessed endovascularly on 2 attempts, whose fistula was successfully closed with SRS, a less invasive modality than endovascular embolization. Fur-ther experience with SRS in this role will be necessary to determine its utility. Journal of Neuro-Ophthalmology 2010;30:138-144 doi: 10.1097/WNO.0b013e3181ceb3e3 2010 by North American Neuro-Ophthalmology Society Carotid-cavernous dural arteriovenous fistulas (CCDAVFs) are abnormal vascular communications between branches of the carotid artery system and the cavernous sinus (1). The natural course of CCDAVFs ranges from spontaneous thrombosis to fatal intracranial hemorrhage (1). Visual deterioration, diplopia, hemor-rhage, headache, orbital symptoms such as intolerable bruit, and significant proptosis are indications for treatment, usually by endovascular embolization (2,3). However, a major disadvantage of endovascular embolization is dif-ficulty accessing the vascular lesion because of the small size and orientation of particular arterial branches relative to the internal carotid artery (4). Because of the success of ste-reotactic radiosurgery (SRS) in the treatment of cerebral arteriovascular malformations (AVMs) (5-7), SRS is now being applied to the treatment of CCDAVFs when these lesions are not accessible endovascularly (8-12). FIG. 1. Before treatment, there is proptosis, eyelid edema, and conjunctival injection of the left eye (top), and the fundus shows dilated retinal veins and hemorrhages (bottom). Departments of Ophthalmology (GTC, MTB), Radiology (SM), Radiation Oncology (JPK), Surgery (Division of Neurosurgery) (AZ, JHS), and Medicine (Division of Neurology) (MTB), Duke University Eye Center and Duke University Medical Center, Durham, North Carolina. John P. Kirkpatrick, MD, PhD is a consultant for Bradmer Phar-maceuticals and has received research support from Varian Medical Systems and lecture fees from Braun Laboratory. Address correspondence to M. Tariq Bhatti, MD, Associate Pro-fessor, Departments of Ophthalmology and Medicine (Division of Neurology), 2351 Erwin Road, Duke University Eye Center, DUMC 3802, Durham, NC 27710-3802; E-mail: tariq.bhatti@duke.edu 138 Chong et al: J Neuro-Ophthalmol 2010; 30: 138-144 Original Contribution Copyright © North American Neuro-ophthalmology Society.Unauthorized reproduction of this article is prohibited. In this report, we describe the use of SRS to treat a CCDAVF recalcitrant to conventional endovascular embolization techniques. CASE REPORT A 54-year-old man with no significant past medical history presented with periocular swelling and a redness of the left eye for several weeks. MRI demonstrated enlargement of the left superior ophthalmic vein. Visual acuity was 20/20 in both eyes. Pupillary reflexes were normal. The left eye displayed 8 mm of proptosis (Fig. 1, top). An orbital bruit could not be auscultated. Eye movements were normal. Slit lamp examination revealed corkscrew configuration of the conjunctival vessels of the left eye. Intraocular pressures were 19 mmHg in the right eye and 26 mmHg in the left eye. Dilated fundus exami-nation was normal in the right eye, and there was engorge-ment of the retinal veins and scattered retinal hemorrhages in the left eye (Fig. 1, bottom). FIG. 2. Before treatment, time-resolved angiography with stochastic trajectories MRA shows early filling of the left superior ophthalmic vein (red arrow) and the left facial vein (blue arrow) due to the carotid-cavernous fistula. Note the later filling of the remaining venous structures, such as the superior sagittal sinus (green arrow). Because of a technical phenomenon (the ‘‘wraparound'' effect), a portion of the patient's common carotid artery appears in the superior portion of the images (yellow arrow) and is not a true representation of the patient's anatomy. FIG. 3. Before treatment, a left internal carotid angiogram (A, early arterial phase; B, midarterial phase; C, late arterial phase) shows premature filling of the superior ophthalmic vein (arrow). Original Contribution Chong et al: J Neuro-Ophthalmol 2010; 30: 138-144 139 Copyright © North American Neuro-ophthalmology Society.Unauthorized reproduction of this article is prohibited. Brain MRA using time-resolved angiography with stochastic trajectories (TWIST) protocol demonstrated abnormal early filling of the left superior ophthalmic vein and facial vein consistent with a CCDAVF (Fig. 2). Catheter-based angiography confirmed the MRA findings (Fig. 3). Endovascular embolization via a transfemoral arterial approach was unsuccessful because of an anomalous vas-cular anatomy preventing optimum migration of the catheter to the site of the fistula. Several weeks later, a sec-ond endovascular embolization by transvenous and superior ophthalmic vein approaches was again unsuccessful at ap-proaching the fistula. SRS was performed on the lesion with a 7-arc plan, using the mini multileaf collimator generated by Radionics XKnife RT software (version 3.0.1; Integra Radionics, Burkington, MA). Treatment with 1,400 cGy was pre-scribed to the 96% isodose line (Fig. 4), yielding a tissue-to- volume ratio (TVR) of 2.5. The patient underwent treatment on a Varian 2100EX linear accelerator (Varian Medical Systems, Palo Alto, CA). Within 3 months of treatment, the patient had re-markable improvement in intraocular pressure, proptosis, conjunctival injection (Fig. 5, top), and venous stasis reti-nopathy (Fig. 5, bottom). Follow-up MRA did not show FIG. 4. Stereotactic radiosurgery plan shows the lesion (A) and the dose distribution (in cGy) in T1 axial (B), coronal (C), and sagittal (D) MRI. FIG. 5. Three months after stereotactic radiosurgery treatment, the congestive features (top) and retinal ab-normalities (bottom) are much reduced compared with the pretreatment photographs (Fig. 1). Original Contribution 140 Chong et al: J Neuro-Ophthalmol 2010; 30: 138-144 Copyright © North American Neuro-ophthalmology Society.Unauthorized reproduction of this article is prohibited. any enhancement of venous structures, indicating closure of the fistula (Fig. 6). DISCUSSION Our patient underwent successful SRS treatment of an endovascularly inaccessible CCDAVF. SRS has been studied sparingly in this capacity (9,10, 13-15). It involves inducing selective vascular injury, resulting in obliteration of the vascular lumen (9). A therapeutic dose of radiation (between 20 and 50 Gy) leads to a variety of vascular changes, including perivascular/ subendothelial edema, fissuring of the vessel wall, spot hemorrhages, thrombi, degeneration and necrosis of en-dothelial cells, increased interstitial colloids, and increased fibroblastic activity (9). Based on 7 published case series, the treatment of CCDAVF with SRS has shown a complete obliteration rate of these lesions that ranges from 50% to 100% (Table 1) (8-13,16). The authors cited the advan-tages of using SRS when the vascular lesion was inaccessible endovascularly or when endovascular treatment would have resulted in a high risk of complications (8-12). A staged, multimodal approach combining endovascular embolization with SRS (12) offers a method of providing the immediate yet sometimes temporary resolving effects of endovascular embolization and the delayed yet permanent benefits of SRS. Most published studies have focused on SRS in the treatment of brain AVMs, which involve the pial vessels (17,18). Unlike brain AVMs, CCDAVFs are extradural and do not have a nidus of hybrid abnormal vessels at their center (1,19). Whether these differences will affect the success of SRS in CCDAVF is unknown. An advantage of SRS over endovascular embolization is its less invasive nature (9). A potential drawback is the latency period of obliteration after treatment, during which patients are at risk for cerebral hemorrhage (20). Fortu-nately, compared with AVMs, CCDAVFs seem to react more promptly to radiosurgery, with the earliest closure observed at 6 months (9). Fractionated radiotherapy may not be as effective (9). An interesting aspect in the management of our patient was the use of TWIST MRA, which showed remarkable visualization of the fistula comparable to the current gold FIG. 6. Three months after stereotactic radiosurgery treatment, time-resolved angiography with stochastic trajectories MRA no longer shows retrograde venous filling. Filling of the facial vein (white arrow) is concurrent with filling of other venous structures, as is the filling of the superior ophthalmic vein (black arrow). Original Contribution Chong et al: J Neuro-Ophthalmol 2010; 30: 138-144 141 Copyright © North American Neuro-ophthalmology Society.Unauthorized reproduction of this article is prohibited. TABLE 1. Published series of stereotactic radiosurgery for closure of carotid-cavernous dural arteriovenous fistulas Study Age Range of Patients (years) No. Patients/ Sex CCDAVF Type* Treatment Before SRS Radiation Dose (Gy) Complications Follow-up Period Outcome Soderman et al. 2006 (8) (Sweden) Not reported 49 patients with 52 cases, gender not reported 16 cases type I (Borden) or types I and IIA (Cognard) 36 cases type II and III (Borden) or type IIa+b, IIb, III, and IV (Cognard) 9 treated with embolization or surgery prior to radiation GKR: average 22 1. One patient: 6th cranial nerve palsy that resolved 2.One patient: late radiation reaction with hemorrhage occurring approximately 10 years after radiosurgery 3. One patient: posterior fossa bleed 2 months after radiosurgery 4. One patient: asymptomatic occipital hemorrhage approximately 6 months postradiosurgery 2 years 41 cases with 2-year follow-up angiography: 28 CO, 10 PO, 3 no change Koebbe et al. 2005 (10) (United States) 50-89 18 (9 F, 9 M) Barrow B, C, and D 9 embolization GKR: mean margin radiosurgery dose was 20 1. One patient: temporary hemiparesis after GKR 2. Two patients: permanent neurological deficits resulting from embolization prior to radiosurgery 2-116 months (mean 43 months) 9 CO, 5 ‘‘smaller on MRI'', 1 died before follow-up, 1 no change but symptoms improved, 2 no imaging Onizuka et al. 2003 (11) (Japan) 67-79 4 (all F) Barrow 3 D, and 1 D!B 1 embolization GKR: 26-30 (max dose) No significant side effects reported 14-32 months (mean 24 months) 4 CO Pollock et al. 1999 (12) (United States) 34-80 20 (17 F, 3 M) Barrow B, C, and D 3 embolization Median marginal radiation dose: 20, median maximum radiation dose: 40 1. One patient: diplopia 2. Two patients: new neurological deficits after embolization procedures 3.One patient: temporary aphasia secondary to a venous infarction 4.One patient: permanent 6th cranial nerve weakness secondary to acute cavernous sinus thrombosis 4-59 months (median 36 months) 13 CO, 1 PO, 1 recanalized, 5 refused follow-up but surgery improved Original Contribution 142 Chong et al: J Neuro-Ophthalmol 2010; 30: 138-144 Copyright © North American Neuro-ophthalmology Society.Unauthorized reproduction of this article is prohibited. TABLE 1. (continued) Study Age Range of Patients (years) No. Patients/ Sex CCDAVF Type* Treatment Before SRS Radiation Dose (Gy) Complications Follow-up Period Outcome Guo et al. 1998 (9) (Taiwan) 29-75 18 (12 F, 6 M) Barrow B, C, and D None GKR: 22-38 (mean 28) No complications reported 6-27 months (median 12 months) 12 CO, 3 PO, 1 died of other causes, 2 no data Barcia-Salorio et al. 1994 (13) (Spain) Not reported 25, gender not reported Barrow B (11), C (4), D (7), T (3, traumatic, high flow) None Conventional radiation therapy: 20-40 Not reported 15 months-14 years (mean 49.76 months) 100% CO of type B, 75% CO of type C, 85.7% CO of type D, 33% CO of type T* Barcia-Salorio et al. 1991 (15) (Spain) Not reported 20, gender not reported Low flow CCF None Conventional radiation therapy: 36-40 Not reported Not reported ‘‘90% cure'' CCDAVF, carotid cavernous dural arteriovenous fistulas; CCF, carotid cavernous fistula; CO, complete obliteration; F, female; GKR, gamma knife radiosurgery; Gy, gray; M, male; PO, partial obliteration; SRS, stereotactic radiosurgery; *T, traumatic, high-flow fistulae with flow reduction after internal carotid trapping (type of CCDAVF based on author's classification). Original Contribution Chong et al: J Neuro-Ophthalmol 2010; 30: 138-144 143 Copyright © North American Neuro-ophthalmology Society.Unauthorized reproduction of this article is prohibited. standard catheter-based angiography (21). Recent advances in dynamic magnetic resonance instrumentation, including an improved signal-to-noise ratio due to the availability of higher field strength magnets and improved temporal res-olution due to the development of parallel imaging tech-niques, have made TWIST an attractive option. However, it lacks the spatial resolution to demonstrate small feeding vessels of CCDAVFs, such as the inferolateral arterial trunk, the meningohypophyseal arterial trunk, and the artery of the foramen rotundum. Detailed information pertaining to the anatomy of the venous system is also not demonstrated owing to limited spatial resolution. Furthermore, dynamic MRA does not allow the demonstration of structural changes and detailed morphology of the cavernous sinuses. 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