We retrospectively reviewed the cases of traumatic carotid cavernous fistulas (CCFs) admitted at Siriraj Hospital between 1993 and 2003. The patients were classified as type A (direct) CCF according to Barrow’s classification.³ÿ Transarterial balloon embolization or other form of embolization, such as transvenous embolization, was chosen as an initial treatment with an effort to preserve the patency of ICA in all patients.ÿIn one patient, the initial treatment was considered surgical direct packing of the cavernous sinus.ÿ In 23 patients, endovascular treatment failed to occlude the fistulas; the patients underwent direct cavernous sinus packing to seal of the fistula. One patient underwent emergency endovascular sacrifice of ICA due to massive nasal bleeding from false aneurysm in sphenoid sinus. The patients were operated by the staff of the Neurosurgery Division, Department of Surgery, Faculty of Medicine Siriraj Hospital.ÿ

Clinical follow ups included outpatient clinic, telephone contact with the patient and an immediate relative or chart review.ÿ Any brain imaging (computed tomography of the head and cerebral angiography) examination performed subsequent to treatment was analyzed, and magnetic resonance (MR) angiography was offered to some patients.ÿ Data were collected and analyzed from medical record, radio-angiographic record, and follow-up results of the combination of treatment.ÿ

Standard detachable balloon technique for the treatment of CCFs begins with systemic heparization (3,000 unit).ÿ An 8 Fr. guiding catheter positioning in the ICA is used followed by mounting a gold valve detachable balloon (Nycomed) on a Minitorquer CIFN. The Goldvalve is a detachable balloon with integrated valve.ÿThe Goldvalve balloons are made from latex with a leak-proof valve and a radiopaque gold marker.ÿThey can be tested and mounted with the blunt needle included in the package.ÿThe balloons are designed to be mounted easily and precisely with optimal safety.ÿThe Minitorquer CIFN is a microcatheter that is used as a carrier catheter.ÿThe Goldvalve detachable balloons must be mounted on specific catheters.ÿ These carrier catheters allow balloon navigation within the vasculature, its inflation and final detachment.ÿAfter entering the cavernous sinus, the balloon is slowly inflated until the fistula is completely occluded.ÿTo adjust the volume of the balloon, injection through the guiding catheter is tested before detachment. In many patients, more than one balloon might be required to obliterate the fistulae.⁵

When arterial sacrifice is being considered as a therapy for traumatic CCF, balloon occlusion test is used to determine if the patient can hemodynamically tolerlate arterial sacrifice.ÿIt evaluates the adequacy of collateral flow, primarily through the circle of Willis. The test requires the use of temporary balloon occlusion of arteries with concomitant electroencephalographic (EEG) and clinical assessment of brain functions.ÿIf the patient tolerates the temporary balloon occlusion for 30 minutes or more, the parent artery is then permanently occluded with detachable balloon or coils.ÿIf the patient fails this functional test, an external carotid-internal carotid (EC-IC) bypass preceeded the permanent arterial occlusion.

Surgical technique of the surgical packing of the cavernous sinus is started by frontotemporal craniotomy with head rotate 30 degree toward the contralateral side.ÿIn addition to routine intraoperative monitoring, a Doppler ultrasound transducer is fixed extracranially on the orbit to record the bruit.ÿProximal control of the cervical common carotid artery (CCA), internal carotid artery (ICA) and external carotid artery (ECA) is secure and surrounded by an elastic band to allow later temporary occlusion.ÿ A combined extradural-intradural approach to the cavernous sinus, as described by Dolenc^13,14 is applied in direct surgical packing of cavernous sinus.ÿExtradural removal of the sphenoid ridge and the anterior clinoid process with intradural unroofing the bone of optic canal are done subsequently.ÿThe ICA is dissected from the ophthalmic artery backward, along the sella turcica. Partial opening of anterior carvernous sinus through Dolenc triangle is done. Packing of anterior carvernous sinus through the anteromedial triangle (Dolenc triangle) is done. Packing of the cavernous sinus with thrombogenic materials (7-10 small pieces of muscle and SurgicelR) along the medial aspect of the ICA is performed gently with Doppler monitoring during the entire procedure until the sound of fistulae was silence.ÿ

The other rout to enter the cavernous sinus is Parkinson’ s triangular area (formed by the third and fourth cranial nerves running together within the dural roof of the cavernous sinus toward the superior orbital fissure and the ophthalmic division of the fifth cranial nerve in the inferior lateral dural wall).^2,11,12 It is safe to open the cavernous sinus without these nerves injury if the incision is carried parallel to and beneath the point of entry of third nerve.

If arterial bleeding should occur, the blood flow can easily be interrupted by placing temporary clips on cervical ICA and distal control at the clinoidal segment of ICA proximal to the origin of ophthalmic artery to avoid the possibility of visual loss.ÿThe proximal ICA is not occluded until distal occlusion is also possible to avoid retrograde vascular steal and possible distal circulation ischemia.ÿThe time for temporary occlusion of ICA during packing the cavernous sinus varies from 15 to 30 minutes.

From 1993- April 2003 we have total 25 cases of combined surgery and endovascular treatment of complicated carotid cavernous fistula.ÿThe ratio of male and female is 20: 5, as men have more exposure to accident, especially motor vehicle accidents.ÿInterestingly, bilateral CCF was noted in three cases.ÿ

The onset of the symptoms was 1 day to 4 months after injury.ÿ Surprisingly, 1 case developed chronic CCF more than 20 years after injury.ÿ Reviewing the causes of trauma, we found the following:ÿ21 cases were motor vehicle accidents, 2 cases car accidents and 2 cases direct blunt injuries.ÿWe analyzed the angiographic findings to identify the cause of unsuccessful treatment by detachable balloon embolization.ÿAs described in Table 1, most common causes of failure of embolization were, namely:ÿ small-hole fistula (9 cases), early deflation of balloon (9 cases) and difficult position of fistulae (3 cases).ÿ

Twenty-three patients were operated by cavernous sinus packing techniques.ÿ As seen in table 2 and 3, there are four cases of failed packing of cavernous sinus (case No. 16, 17, 21, and 24).ÿThree of four of the cases, ICA were occluded by balloon occlusion and surgical tapping of ICA without neurological deterioration from ischemic event.ÿWe have one CCF patient who was decided to be operated by packing the cavernous sinus because angiographic machine was unavailable at that time and rapid progressive visual loss (case 24). At first, the surgical packing of cavernous sinus failed, but attempt endovascular embolization of the CCF was subsequently successful.ÿ In two patients, bypass operation had to be performed due to false aneurysm and ischemic neurological deficits (case 18 and 23). In case 18, the patient went into coma due to a massive nasal bleeding from false aneurysm into sphenoid sinus.ÿBecause of emergency situation, balloon sacrifice of right cavernous ICA was performed in order to save life.ÿOne week after, he developed left-side weakness after recovering from the coma.ÿThe bypass operation (right cervical ECA to supraclinoid ICA) was selected to augment the cerebral blood flow. In case 23, the patient had bilateral traumatic CCF and false aneurysm of left cavernous ICA projecting superiorly with tendency of rupture.ÿFirstly, right balloon embolization was attempted to cure right CCF and to preserve right ICA and left ICA sacrifice was planned to cure the CCF and false aneurysm after balloon occlusion test of left side had been successful. Unfortunately, the right CCF was came again after early deflation of balloon.ÿSo, the bilateral ICA was surgically trapped after bypass surgery between right cervical ECA and supraclinoid ICA had been done successfully. These two patients with bypass surgery were no further neurological deficit after complete treatment.

All 25 patients had good results with completed resolution of clinical triad symptoms, obliteration of fistula in 23 of patients, partial obliteration of fistula in 2 patients.ÿBy follow-up cerebral angiography of 16 patients performed cavernous sinus packing, we could preserve the patency of ICA in 8 patients but 5 patients had thrombosis of ICA without ischemic events.ÿ In 3 patients (case No. 16, 17, and 21), an operation to occlude the ICA after failure of cavernous sinus packing was performed.ÿ There was no immediate neurological deficit with absent of CCF.ÿAnyway, the long-term MRI study of patient No. 15 who had thrombosis of left ICA had shown atrophy of left cerebral hemisphere without motor deficit or dysphasia.

Illustrate cases

Case 1ÿ

A 43-years-old Thai female had right chemosis, proptosis, and bruit in the right eye after a head trauma.ÿRight CCF was diagnosed by an ophthalmologist.ÿHead CT showed enlarged cavernous sinus after contrast enhancement (Fig 1A).ÿDefinite diagnosis of CCF was confirmed by cerebral angiography that revealed a small-hole fistula at the junction of C4 and C5 portion of ICA and narrowing of inferior petrosal sinus (Fig 1B).ÿAccordingly, the microcatheter could not be passed through the hole of fistula due to its difficult position (Fig 2A). Right craniotomy for cavernous sinus packing was performed after a failed balloon embolization.ÿPostoperatively, eye symptoms and signs were subsiding immediately and MR imaging and angiography demonstrated no residual CCF and the patency of ICA lumen was maintained (Fig 2B).

Case 3

A 32-years-old Thai female developed right CCF early as two weeks after the car accident.ÿShe had right chemosis, proptosis, and bruit in the right eye.ÿSurprisingly, there are spontaneous regressions of proptosis and chemosis but still bruit. Cerebral angiography showed a small-hole fistula at dorsal aspect of C3-C4 portion of the ICAÿ without ophthalmic venous drainage which explain the regression of eye sign (Fig 3A).ÿBalloon embolization was planning to obliterate the fistula.ÿUnfortunately, both of transarterial and transvenous balloon embolization were unsuccessful because the hole of fistula was too small and the catheter could not pass through a narrow petrosal sinus (Fig 3B). Cavernous sinus packing with small pieces of muscle and SugicelR was done with the technique of extradural Dolenc approach using intraoperative angiography.ÿPostoperative cerebral angiography revealed patency of cavernous sinus ICA and complete obliteration of the fistula (Fig 3C).ÿ

Case 9

A 29-year-old man was brought to the hospital due to alteration of consciousness. On examination, he had the clinical triad of left eye.ÿHead CT revealed diffuse subarachnoid hemorrhage and intraventricular hemorrhage.ÿThe diagnosis was made after cerebral angiography had been done (Fig 4A).ÿSurprisingly, a left small aneurysm proximal to the junction of posterior cerebral artery and posterior communicating artery was seen (Fig 4B) with the present of left CCF.ÿAfter he was recover from subarachnoid hemorrhage, detachable balloon embolization was performed using 3 balloons (Fig 8A, B). The patient was immediately relieved from symptoms.ÿTwo days later, he felt the previous symptoms again.ÿ Due to early deflation of the balloon, direct surgical packing of the cavernous sinus was attempted.ÿBut the fistula had been persisting after the operation.ÿ Successful second balloon embolization was done using 4 balloons.ÿPostembolization cerebral angiography was done 1 month later.ÿThe CCF was cure with small venous pouch and a small aneurysm could not be seen anymore (Fig 4C).

Anatomy and pathophysiology of the traumatic carotid carvernous fistulas (CCFs)

Cavernous sinuses are a paired venous structure in the anterior portion of the middle cranial fossa. They located on either side of the sella turcica and the pituitary gland received blood supply from the superior and inferior ophthalmic veins and sphenoparietal sinuses.ÿThe venous drainage from the cavernous sinuses enters the superior and inferior petrosal sinuses and eventually drains into the transverse sinus. The paired dural venous structure connected via small venous channels as known as inter-cavernous sinuses.^6,7 Fractures or the shearing forces of severe head trauma may cause weakness of the of the ICA or cause an actual laceration producing a vascular shunt from a high-flow arterial system into a low-flow venous sinus, resulting in CCFs.⁸ The high venous pressure causes a “back-up” pressure to the venous drainage of the cavernous sinus resulting in orbital triad symptoms (proptosis, chemosis and bruit).⁶ÿIn case of aggressive type of carotid cavernous fistulas, there are retrograde venous refluxes to the cortical venous system.ÿAccordingly, they may cause cerebral venous ischemia from retrograde venous hypertension and congestion.

Anatomy of internal carotid artery and approaches to the cavernous sinus

Fischer assigned the classification of ICA using the carotid bifurcation as the starting point (Fig. 10).ÿMost distal portion (C6) is defined as the intrapetrous portion of the internal carotid artery.ÿThe C5 portion is short segment between the fibrous ring and the posterior bend of the vessel.ÿThe junction of the C4 and C5 segments is the meningohypophyseal trunk. The C4 segment of the artery is horizontal toward the superior orbital fissure and exits the cavernous sinus by piercing the carotico-oculomotor membrane to enter the epidural space under the anterior clinoid process.ÿThe C3 segment, also known as the “siphon” or “clinoid segment”, bends posterior and superior to penetrate the dura.ÿÿÿÿ

History of the treatment of carotid cavernous fistula (CCF)ÿ

Traumatic carotid cavernous fistulas (CCFs) are the neurosurgical disease. In the past, definitive treatment of CCFs was usually performed by neurosurgeons.ÿThe treatment of CCF has undergone a dramatic evolution from a wholly surgical approach to one that now uses embolization techniques initially and reserves surgery for cases in which intravascular method fail.ÿ

The pathological entity was first described 200 years ago.ÿIn 1809, Travers treated this lesion by ligating the common carotid artery for pulsatile exophthalmos in a 34-year-old pregnant woman.⁶ÿÿIn 1931, Brooks embolized a piece of muscle into a CCF via the ICA.ÿ In 1964, Hamby used a combination of embolization of muscle and intracranial ICA ligation to close CCFs.^9ÿ

In 1965, Parkinson pioneered direct surgical exposure of the intracavernous ICA through the lateral wall of the cavernous sinus (Parkinson’s triangle) with the aid of hypothermic cardiac arrest.2ÿÿIn 1974, Mullan introduced hemostatic agents, such as gelfoam and oxidized cellulose, directly into the exposed cavernous sinus through its draining veins.¹⁰ In 1983, Dolenc described his approach to expose of the entire cavernous sinus for the treatment of direct CCF.^13,14

Serbinenko revolutionized the therapy for CCF in the 1970s by introducing detachable intravascular balloons.¹⁵ÿEndovascular detachable balloon occlusion of CCF introduced through a transfemoral access allows preservation of the distal aspect of the
ICA. This method is the current standard therapy in most cases of CCF.^16-19ÿIn addition to the transfemoral detachable balloon embolization, several other modalities have been deemed useful in the treatment of CCFs in recent years.ÿ Transvenous embolization via the superior ophthalmic vein, the double-balloon embolization technique, and coil embolization modalities have been used with various success rates.^20-22 In fact, some clinicians believe that unless urgent treatment is indicated (i.e., rapid loss of vision, progressive hemiplegia, herniation of cavernous sinus into the sphenoid sinus), 6-week delay and a repeat angiogram may be prudent before embarking on an intervention.²³

Results and complication of detachable balloon embolizationÿÿÿ

However, failure to embolize the CCF may occur on a few occasions, such as when the balloon cannot pass through the fistula into the cavernous sinus by blood flow, or when the inflated balloon in the cavernous sinus retracts to the carotid artery.ÿUnder these circumstances, the ICA may have to be sacrificed in order to treat the CCF.^23,24 Complications associated with endovascular therapy (e.g., thromboembolic and ischemic events, pseudoaneurysm formation, and alteration of arterial flow resulting in hemorrhage, edema, or worsening of ocular symptoms) are not frequent.²⁵ÿHantson P, et al. reported one patient who developed brain edema leading to death after detachable balloon embolization of bilateral CCF. They postulated that reestablishment of normal cerebral perfusion after abrupt closure of the fistulas might have played a deleterious role.²⁶ÿ Senser S and colleague reported diplopia associated with balloon migration on the venous side of the treated CCF.²⁷

Surgical Strategy for the treatment of the traumatic CCFs

The treatment modalities for traumatic CCFs included ligation or trapping of the carotid artery, muscle embolization via cervical exposure of the carotid system, and balloon embolization combined with carotid artery ligation and direct surgical intervention. Thanapura C reported 12 patients of traumatic CCFs who were cured under circumstances such as the lack of angiography, poor socio-economic status, or patients wanting to be treated close to home.²⁸ÿÿAll of the patients were treated by muscle embolization only; muscle embolization with internal carotid ligation (Brooks technique); muscle embolization with trapping (Jaeger-Hamby procedure); or muscle embolization with trapping and external carotid ligation.ÿHowever, the problems of these treatments are, namely:ÿ risks of ischemia from ICA occlusion, visual loss and recurrent of the fistula.ÿTo date, dramatic treatment of CCF has changed with the evolution of interventional radiography.ÿ

Neuroangiographic studies of the CCF are completed before the operation.ÿIn case of total steal of ICA blood flow should predict the tolerances after ICA sacrifice.ÿBalloon occlusion test (BOT) was not performed in all patients.ÿFailure to pass the BOT when ICA occlusion is required for CCFs control which may need an extracranial-to-intracranial bypass surgery.ÿDespite a negative preoperative test occlusion, neurological deficits can occur after endovascular sacrifice of the ICA, the rate of permanent post-procedural neurological deficits varies from 0% to 10%.^29,30ÿ Moreover, the goal of treatment of traumatic CCFs should cure the fistula, preserve the patency of blood flow via the ICA and restore neurological function.

Tu YK, et al. reported a series of direct surgery of carotid cavernous fistulae and dural arteriovenous malformations of the cavernous sinus.ÿThe patients had embolization problems such as large fistula, tiny fistula, multiple fistulae, site of fistula which difficult to thread the catheter, several recurrences and acute bleeding of a false aneurysm.ÿSixteen patients with type A or direct carotid cavernous fistula underwent direct intracavernous repair of carotid cavernous fistulae.ÿHalf of the patients (8/16) were treated by sinus packing, one patient underwent sinus packing and intracranial-intracranial (IC-IC) bypass operation, two patients underwent IC-IC bypass operation, three patients were treated by sealing the fistulae with fascia and acrylate glue and one patient with multiple fistulae underwent suture and clipping operation.ÿThey found that one-fourth (4/16) of the patients had ICA thrombosis.ÿAs compared to our series, we have one-fifth (5/25) of the patients who had ICA thrombosis.ÿBut the incident of ICA thrombosis in our series should be more than 5 patients because 7 patients did not have the postoperative angiography.ÿThe etiology of ICA thrombosis after packing cavernous sinus may be compromise the ICA patency by over-packing of the cavernous sinus.³¹ÿÿ