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 Table of Contents  
Year : 2019  |  Volume : 52  |  Issue : 6  |  Page : 221-228

Linear accelerator-based radiosurgery in treating indirect carotid cavernous fistulas

1 Department of Neurosurgery, Linkou Chang Gung Memorial Hospital, Chang Gung University, Taoyuan, Taiwan
2 Department of Medicine, College of Medicine, Chang Gung University, Taoyuan, Taiwan
3 Department of Radiology, Linkou Chang Gung Memorial Hospital, Chang Gung University, Taoyuan, Taiwan
4 Department of Neurosurgery, Keelung Chang Gung Memorial Hospital, Chang Gung University, Keelung, Taiwan

Date of Submission23-May-2019
Date of Decision25-Jun-2019
Date of Acceptance19-Aug-2019
Date of Web Publication05-Dec-2019

Correspondence Address:
Dr. Peng-Wei Hsu
Department of Neurosurgery, Linkou Chang Gung Memorial Hospital, No. 5, Fuxing St., Guishan Dist., Taoyuan City 33305
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/fjs.fjs_43_19

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Introduction: The purpose of this study is to determine the success and complication rates of linear accelerator (LINAC)-based radiosurgery (X-knife) for indirect carotid-cavernous fistulas (CCFs).
Materials and Methods: This retrospective study was performed at the Department of Radiosurgery, Chang Gung Memorial Hospital, Taiwan, and reviewed data from May 2006 to May 2018. Thirteen patients with CCF who were treated with stereotactic radiosurgery were included, and side, volume, pathological type, origin, location, postoperative regression, and recurrence rate were evaluated with postradiotherapy. Patients were either followed up with contrast magnetic resonance imaging or angiography. Radiosurgery was considered successful if the patients' clinical symptoms improved with radiological remission or if there was a reduction in CCF flow in angiography.
Results: Of the 11 patients, three (27.3%) received transarterial embolization (TAE) before radiosurgery. Successful radiological outcomes were seen in 10 (90.9%) patients, and the remaining one patient (9.1%) had stationary disease with no reduction in CCF flow. Ten patients (90.9%) had improved clinical symptoms; however, one patient (9.1%) was complicated with iatrogenic blindness after TAE treatment. No acute or subacute transient postradiation changes, optic nerve injuries, or brainstem radionecrosis were noted in any of the patients.
Conclusions: In this study, LINAC-based radiosurgery for CCF was found to be an effective, safe, and successful treatment alternative to TAE treatment in patients with indirect CCF. The risk of postradiotherapy complications was low, and obliteration and regression rates were high.

Keywords: Carotid-cavernous sinus fistula, dural, stereotactic radiosurgery, X-knife

How to cite this article:
Ong TC, Lin PY, Wu CT, Siow TY, Chuang CC, Chang CN, Chen HC, Liu ZH, Lu YJ, Tsai HC, Hsu PW. Linear accelerator-based radiosurgery in treating indirect carotid cavernous fistulas. Formos J Surg 2019;52:221-8

How to cite this URL:
Ong TC, Lin PY, Wu CT, Siow TY, Chuang CC, Chang CN, Chen HC, Liu ZH, Lu YJ, Tsai HC, Hsu PW. Linear accelerator-based radiosurgery in treating indirect carotid cavernous fistulas. Formos J Surg [serial online] 2019 [cited 2021 Jul 24];52:221-8. Available from: https://www.e-fjs.org/text.asp?2019/52/6/221/272316

  Introduction Top

Introduction of carotid-cavernous sinus fistulas

Carotid cavernous fistulas (CCFs) are characterized by abnormal arteriovenous communication between arteries and veins of the CS.[1] Direct fistulas are characterized by a direct connection between the internal carotid artery (ICA) and the CS. They are usually high-flow fistulas, resulting from penetrating or blunt trauma, rupture of an ICA aneurysm within the CS, Ehlers–Danlos syndrome Type IV, or iatrogenic interventions, including transarterial endovascular interventions, internal carotid endarterectomy, percutaneous treatment of trigeminal neuralgia, transsphenoidal resection of a pituitary tumor, and maxillofacial surgery.[2],[3],[4],[5] Indirect CCFs consist of a communication between the CS and cavernous arterial branches and usually present with a benign clinical course and a low risk of intracranial hemorrhage because retrograde cortical venous drainage (CVD) is uncommon.

The decision on whether to treat depends on lesion- or patient-specific factors, location, angiographic features, and clinical presentations.[6],[7],[8] Some CCFs may resolve spontaneously with conservative treatment. Endovascular embolization is currently the treatment of choice for rapid symptom relief; however, incomplete obliteration, recanalization, and complications are always observed after treatment.[9] Recently, stereotactic radiosurgery (SRS) has emerged as an alternative primary management option for patients with CCFs who cannot tolerate the risk of embolization due to its minimal invasiveness, higher total obliteration rate, and fewer complications.[10],[11],[12]

Classification of CCFs

A CCF can be classified as being either direct or dural (indirect). Direct CCFs are characterized by a direct connection between the ICA and CS, whereas dural CCFs (DCCFs) result from an indirect connection involving cavernous arterial branches and the CS.[13]

DCCFs are classified according to the systems proposed by Borden et al.,[14] Cognard et al.,[15] and Barrow et al.[1] The Borden classification is based on the site of venous drainage and the presence or absence of cortical vein drainage.[14] The Barrow classification of DCCFs is based on direct fistulas (Barrow type A) and dural or indirect fistulas (Barrow types B, C, and D).[1] Barrow type B fistulas involve meningeal branches of the ICA, Barrow type C fistulas involve external carotid branches, and Barrow type D fistulas include meningeal branches from both the ICA and external carotid artery. The most prevalent form of indirect CCF is type D.[16]

The Cognard classification system[15] is based on the direction of dural sinus drainage, the presence or absence of CVD, and venous outflow architecture, and includes Type I, drainage into dural venous sinus with antegrade flow; Type IIa, drainage into dural venous sinus with retrograde flow; Type IIb, drainage into dural venous sinus with antegrade flow and CVD; Type III, direct drainage into cortical vein without venous ectasia; Type IV, direct drainage into cortical vein with venous ectasia; and Type V, direct drainage into spinal perimedullary veins.

  Materials and Methods Top

Patient population

We conducted this retrospective analysis at a single institution, and the study was approved by the institutional review board of Chang Gung Memorial Hospital, Taoyuan, Taiwan (IRB No. 201700082B0 obtained on Feb 8th, 2017). IRB agrees to waive the informed consent. Data were reviewed from May 2006 to May 2018. We analyzed the radiologic and clinical outcomes of 13 consecutive patients with indirect CCFs who underwent SRS at our institution. The diagnoses of DCCFs were confirmed by performing either digital subtraction angiography (DSA) or magnetic resonance angiography (MRA). Bilateral selective ICA angiography, external carotid artery (ECA) angiography, and vertebral artery angiography were performed in 11 patients to assess the feeding arteries, venous drainage, and site and size of the fistulas. Two patients received DSA at other hospitals and received SRS at our hospital without further radiologic examinations. We excluded two patients due to last DSA and/or because MRA follow-up was <6 months.

We evaluated the efficiency and efficacy of SRS for indirect CCFs (Barrow Type B [n = 2] and D [n = 9]) with nontraumatic spontaneous bleeding. A symptomatic DCCF was defined as eye swelling, eye congestion, eye redness, sclera and conjunctiva ecchymosis, double vision, and/or blurred vision. Perioperative side effects including acute transient change (<24 h) and subacute change (<7 days) were recorded. We also evaluated the side, volume, pathological type, origin, location, postoperative obliteration, partial obliteration (regression), and recurrence rate with postradiotherapy. Patients with direct CCFs, recent history of conventional radiation therapy, and traumatic CCFs were excluded from the study.

Radiosurgical technique

SRS involves the use of a precise highly focused energy X-ray beam to destroy tissue in the brain. It is a method of delivering more accurately targeted radiotherapy than standard radiotherapy. This noninvasive surgical technique does not involve blood loss and has been proven to be an effective alternative therapy for surgery or conventional radiation therapy for the treatment of many tumors and some vascular diseases such as CCF.[17]

The two main elements of the Novalis X-Knife system (Novalis system, Brainlab, Olof-Palme-Straße 9, Munich, Germany) are radiation produced from a small linear particle accelerator and a robotic arm. The robotic arm consists of a 6-MV linear accelerator (LINAC), along with a pair of orthogonal diagnostic X-ray tubes. Continual image guidance technology and robotic mobility tracks detect and correct for tumor and patient movement during treatment. High-dose radiation and pinpoint precision minimize damage to healthy tissue.[18]

The Novalis Radiosurgery System used at our hospital outperforms other radiosurgery techniques by eliminating the need for stereotactic head frames. It delivers high doses of radiation to lesions with great accuracy and treatment errors of <0.1 cm. Thus, the accuracy of the X-knife is high and the dose can be projected by more than 1560 beams, and yet has a very fast “fall-off” dose at the periphery of the carefully mapped target. Therefore, the system enables doctors to achieve a high level of accuracy in a noninvasive manner and allows patients to be treated on an outpatient basis. In this study, we analyzed the efficacy of SRS in improving ocular symptoms and radiographic and clinical outcomes of successful obliteration of CCFs.

Follow-up examinations

Patients underwent clinical outpatient follow-up 1–3 months after SRS. Follow-up DAS and/or MRA were performed according to the patients' informed consent. A physical examination including neurologic and ophthalmic evaluations was performed to assess clinical outcomes at the time of imaging. The patients were asked to describe the severity of their symptoms before and after SRS. An improvement in clinical symptoms after radiosurgery was defined when the neurologic and ophthalmic symptoms were better than that before radiosurgery. Complete recovery was defined as return to normal function with clear evidence of clinical signs, and these patients were defined as having clinically successful outcomes. After SRS, all patients were advised to undergo DSA and/or MRA to evaluate occlusion of the DCCFs. Total obliteration of a DCCF was defined as elimination of the fistulas and the absence of an early draining vein. Subtotal obliteration was defined as regression of the DCCF and decreased flow in the drainage vein. Both total obliteration and subtotal obliteration in DSA or MRA were grouped as radiological successful outcomes. All patients were followed up for a minimum of 6 months (median, 26.0 months; range, 7–90 months).

  Results Top

We evaluated 13 patients with CCFs who underwent SRS from 2006 to 2018 [Table 1]. We exclude the patient 7th and 12th due to last follow-up subtraction angiography and/or MRA in <6 months, although they already achieved complete and/or subtotal obliteration. The median age of the patients at surgery was 59 years (range, 30–80 years). Six of the patients were female and five were male. Five CCFs were located on the left side (45.5%), and six DCCFs were located on the right side (54.5%). The CCFs were idiopathic in all patients and included Barrow Type B in two patients and type D in nine patients. All the patients had ocular signs and symptoms, including eye redness in five patients (27.8%), diplopia in five patients (27.8%), blurred vision in two patients (11.1%), eye swelling in three patients (16.8%), chemosis in one patient (5.5%), sclera ecchymosis in one patient (5.5%), and eye congestion in one patient (5.5%).
Table 1: Summary of 13 patients and treatment characteristics with dural carotid-cavernous fistulas

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All patients underwent SRS for DCCFs as the primary treatment modality, and three (23.1%) patients received transarterial embolization (TAE) prior to SRS according to patients' wish. The median target volume was 1.9 cm3 (range, 0.43–3.7 cm3), and the median treatment dose was 18 Gy (range, 12–20 Gy, 100% dose level was used to cover the lesion margin) depending on the CCF location, type, and clinical features. The optic nerve and brainstem dosages were <8 Gy and <12 Gy, respectively. Thus we ensured that the optic nerve or brainstem received no more than 8 and 12 Gy of radiation.

Ten patients (90.9%) had improved clinical symptoms; however, one patient (9.1%) was complicated with iatrogenic blindness after TAE, and one patient still had persistent blurred vision after SRS. Ten patients (90.9%) had successful radiologic outcome results, and one patient (9.1%) had stationary disease with no reduction in CCF flow.

  Discussion Top

Diagnostic images

Patients with suspected CCF require high-sensitivity neuroimaging such as noninvasive computed tomography angiography (CTA) or MRA.[19] Chen et al.[20] retrospectively studied 53 patients, all of whom underwent pre- and postcontrast enhanced CTA and DSA and 50 patients also underwent MRA. Using the different procedures to detect CCFs, the neuroradiologists found that CTA did not differ significantly from DSA (sensitivity, 87% vs. 94.4%), whereas the sensitivity for MRA was significantly lower (80%). As a result, patients in whom a CCF is suspected such as with an enlarged superior ophthalmic vein on standard computed tomography or magnetic resonance imaging (MRI) may still require DSA.[21] DSA remains the gold standard for the classification and diagnosis of CCF, and it can be both diagnostic and therapeutic.[22] In addition, DSA characterizes the drainage pattern of the fistula, which can determine whether there is reflux into cortical veins.[19]


With the development of endovascular interventional techniques, the range of potential therapies has broadened. Accordingly, open surgical procedures are no longer preferred, and the ICA can almost always be preserved. Compared with ICA sacrifice, endovascular treatment is less invasive and carries a lower risk of cerebral infarction.[9] The ideal treatment approach depends on the arterial supply, venous drainage, speed of blood flow through the fistula, and patency of the circle of Willis.[22],[23]

Even though endovascular intervention offers a 90%–100% cure rate,[24],[25],[26] the major complications such as hemiparesis and permanent ocular motor nerve palsy are the risk in the general population. It still carries the potential risk of neurologic deficits due to ischemic complications and migration of embolic material. Cranial nerve signs after embolization can be caused by progressive thrombosis of the CS, mass effect from the coils, or direct injury to the nerve by the coils or microwire/microcatheter.[27] Patients with underlying vascular fragility such as Ehlers–Danlos Type IV have much higher complication rates with both diagnostic and therapeutic endovascular procedures.[28]

Stereotactic radiosurgery

SRS offers an excellent first-line treatment option with high rates of symptomatic relief and very low complication rates for patients with DCCFs without cortical venous reflux.[29] It targets either the arterial feeders or the nidus, causing radiation-induced changes and ultimately obliteration of the shunt. SRS causes progressive intimal hypertrophy of the vascular wall with subsequent thrombosis of the DCCFs. DSA remains the gold standard for evaluating the precise angio-architecture and flow patterns of DCCFs before and after radiosurgery. For conformal dose planning, it is important to accurately define the nidus using stereotactic angiography and MRI. Hanakita et al.[30] suggested that the targeted area should be limited to the sites of arteriovenous communication. All fistulas located along the sinus wall were included in the radiation target to increase the obliteration of DCCFs. In particular, the target point of radiosurgery for Barrow-Type D CCF included the lateral wall and inferior wall compartments of the CS supplied by multiple feeders from the ECA.

Gamma knife radiosurgery has proved as an effective treatment for low-flow DCCF with multiple shunts.[31] At our hospital, we used frameless LINAC-based SRS to treat the patients. All patients underwent high-resolution MRA, followed by angiography. The images of thin-cut MRI and two-dimensional cerebral angiography of anteroposterior/lateral projection were transferred to a computer workstation, and image fusion was made automatically using the software Brainscan, version 5.31 Brainlab (Olof-Palme-Straße 9, Munich, Germany) for dose planning. Target was outlined using the optimized imaging integration of angiography and MRI. Target volume was determined with fusion images to envelop the three-dimensional nidus volume in a highly conformal and selective dose plan.

Treatment modality

Conservative treatment is often recommended for patients with asymptomatic DCCFs because of their spontaneous regression.[32] Some CCFs without CVD have a benign natural presentation and can be managed conservatively. However, DCCFs associated with venous hypertension, hemorrhage, or nonhemorrhagic neurologic deficits may require transarterial or transvenous endovascular embolization.[33]

Yoshida et al.[34] reported that 7% of their patients had permanent complications and 14% had transient morbidity after transvenous embolization. According to a literature review, minor transient complications including hematoma, facial pain, and ocular motor nerve palsies occur in 1%–30% of cases.[23] Major sequelae including hemiparesis and permanent ocular motor nerve palsy are quite rare in the general population. Meanwhile, the success rate for transvenous procedures is about 80%, with a center-dependent complication rate of up to 20%.[34],[35],[36],[37],[38] Reported complications include ocular motor nerve palsy, trigeminal sensory neuropathy, brainstem infarction, significant intraocular pressure elevation, intracranial hemorrhage, pulmonary emboli, and orbital hemorrhage with an superior ophthalmic vein or inferior ophthalmic vein approach.[34],[37],[38],[39],[40]

In addition, surgical treatment consisting of trapping the fistula by ligating the cervical ICA proximal to the fistula and the intracranial ICA distal to the fistula or occlusion of the common carotid artery or ICA[41] can result in a cerebral ischemic event due to an induced low-flow state or an embolic event.[34],[42]

In this study, we evaluated indirect CCFs (Types B, C, and D) which typically have low-flow rates. The major arterial supply to indirect fistulas arises from the internal maxillary, middle meningeal, accessory meningeal, and ascending pharyngeal branches of the ECA and the meningohypophyseal trunk arising from branches of the ICA.[31] Compared to direct CCF as first-line treatment which involves transarterial or transvenous endovascular embolization,[43] embolization of indirect CCFs is not always possible or effective because of poor vascular access, risk of retrograde flow of embolic materials, or partial embolization.

SRS is recommended for symptomatic indirect CCFs as first-line treatment when surgical or endovascular access is difficult, when there is incomplete obliteration after other treatment modalities, and when there are associated treatment-related risk factors. In this study, indirect CCFs suitable for analysis were identified from our SRS database and were confirmed on imaging studies conducted by a neuroradiologist. Outcome data were collected through an independent medical record review and were analyzed by a neurosurgeon who did not participate in patient management.

Taken together, we suggest that SRS can be an alternative treatment option for indirect CCFs without concurrent fatal conditions such as intracranial hemorrhage or neurological deficits. In addition, we suggest that SRS can be used as first-line therapy when embolization or surgery cannot be performed safely or for residual or recurrent lesions after prior treatment.[44]

Radiological and clinical outcomes

Five lesions (45.5%) got a total obliteration of the CCF and five of them got a subtotal obliteration [Figure 1] and [Figure 2].
Figure 1: Anteroposterior (a) and lateral (b) views of the left external carotid artery angiogram for a left dural carotid-cavernous fistula before radiosurgery. Dose planning (c) showing integration of stereotactic angiography and magnetic resonance images. The dural carotid-cavernous fistula was treated with 15 Gy. Anteroposterior (d) and lateral (e) views after radiosurgery revealing total obliteration of the dural carotid-cavernous fistula in the left external carotid artery angiogram obtained at 25 months

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Figure 2: Anteroposterior (a) and lateral (b) views of the right external carotid artery angiogram for a right dural carotid-cavernous fistula before radiosurgery. Dose planning (c) showing integration of stereotactic angiography and magnetic resonance images. The dural carotid-cavernous fistula was treated with 16 Gy. Preradiosurgery magnetic resonance angiography (d) and postradiosurgery magnetic resonance angiography (e) revealing subtotal obliteration of the dural carotid-cavernous fistula (arrow) at 13 months

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With regard to clinical outcomes, eight patients (72.7%) who did and did not receive TAE before SRS showed improvements, and none of the 11 patients had acute reactions or subacute changes after SRS. Persistent ocular signs and symptoms including persistent blurred vision in one patient (9.1%) and blindness after TAE in one patient (9.1%) were noted; however, neither was caused by SRS. No recurrent DCCFs were noted in any of the patients after SRS.

Complications after treatment for dural carotid-cavernous fistulas

Complications after treatment for DCCFs may result from embolization or radiosurgery. Endovascular embolization carries the potential risk of neurologic deficits because of ischemic complications and migration of embolic material.[24] Overall, none of our patients experienced radiation-related complications or worsening of their symptoms, and no optic neuropathy or hemorrhage was noted after SRS. In addition, no differences were observed in recovery from neurologic symptoms according to age, sex, CCF location and classification, symptom duration, time until symptom improvement and obliteration, presenting symptoms, volume, or radiation dose (data not shown).

Similar to our results, Hanakita et al.[30] reported that none of their patients experienced radiation-induced complications after SRS. Therefore, SRS appears to be an effective and safe primary treatment modality for indirect CCFs with high obliteration rate and low risk of complications. The high accuracy of X-knife SRS also means that the surrounding normal tissues only receive a small fraction of the high central dose of therapy. In addition, the patients only need to undergo one SRS session lasting between 60 and 90 min, compared with the conventional radiation therapy in which the patients have to undergo more than ten sessions, with each session lasting 10–20 min. Thus, X-knife SRS improves the efficiency of treatment by reducing the number of hospital visits and the waste of medical resources.[11],[31]

In addition, radiation therapy often causes discomfort, nausea, and loss of appetite. With X-knife radiosurgery, the side effects vary from patient to patient, with most patients experiencing minimal side effects which often resolve within 1 or 2 weeks. In this study, no acute transient or subacute changes were noted after the treatment. The doctor discusses with the patient all possible side effects they may experience such as mild headache. The doctor may also prescribe medications designed to control any side effects should they occur.

  Conclusions Top

Although transarterial or transvenous endovascular embolization is the treatment of choice for CCFs, it is not always possible or effective because of poor vascular access, risk of retrograde flow of embolic materials, or partial embolization.[34] SRS has become a reasonable alternative treatment option for CCFs without concurrent fatal conditions such as intracranial hemorrhage.[18] SRS can be the first-line therapy when embolization or surgery cannot be performed safely or for residual or recurrent lesions after prior treatment. Our results indicate that SRS is an effective and safe primary treatment modality for CCFs with a high obliteration rate and low risk of complications.

LINAC-based SRS (X-knife) allows for the precise delivery of a high dose of radiation while minimizing radiation injury to normal tissue (optic nerve, brainstem, and cranial nerves III, IV, V, and VI) and can be used as an alternative, safe, and efficient treatment for spontaneous symptomatic CCFs.

We strongly recommend X-knife SRS as a safe, effective, and efficient alternative to surgical procedures for CCFs. It has a very low risk of postradiotherapy complications compared to conventional radiation and surgery treatment.

Financial support and sponsorship

Chang Gung Memorial Hospital provided financial support (grants CIRPG3D0011, CIRPG3D0012, and CIRPG3D0013).

Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2]

  [Table 1]


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