Treatment of direct carotid cavernous fistula with Willis covered stent with midterm follow-up

Abstract

Background

Willis covered stent is the first stent designed exclusively for intracranial vasculature and its application in carotid cavernous fistula is limited. The aim is to evaluate the feasibility and efficacy of this device in treating direct carotid cavernous fistula.

Methods

10 consecutive patients with direct carotid cavernous fistula were treated in our institution with Willis covered stents from September 2013 to December 2015. The characteristics of these patients and the immediate and follow-up results were retrospectively reviewed.

Results

Of the 10 patients, 8 were treated for the first time, and 2 had been treated elsewhere. Willis covered stents were successfully released in 9 patients. Abnormal arteriovenous shunt disappeared in 6 cases immediately after stent deployment and endoleak occurred in 3 cases. Endoleak disappeared at 6-month angiography follow-up in one case and was sealed with coils through a pre-set microcatheter in another case. Parent artery was sacrificed as endoleak remained despite repeated balloon dilation and a second stent deployment in the third case. All patients got clinical follow-up for at least 24 months and 7 patients received angiographic follow-up. Symptoms relieved gradually in all cases except for slight oculomotor paralysis and visual acuity in one case, respectively. In-stent stenosis was found in 1 case and no recurrence was observed.

Conclusions

Willis covered stent is feasible for direct carotid cavernous fistula.

Introduction

Direct carotid cavernous fistula (CCF) is featured by a direct shunt between the internal carotid artery (ICA) and the cavernous sinus, which mainly results from head traumas that damaged the cavernous ICA. Spontaneous direct CCF may also occur after rupture of a cavernous ICA aneurysm. The typical clinical manifestation of a direct CCF is a triad consisted of pulsating exophthalmos, chemosis and visual loss. Stealing of the blood may result in hypoperfusion of the ipsilateral hemisphere and the drainage pattern determines the hazardous consequences of the disease. Cortical superficial vein drainage may cause lethal intracranial hemorrhage.

The optimal goal for treating CCFs is to occlude the abnormal shunt and preserve ICA patency. In 1973, Parkinson first reported surgical repair of direct CCFs with parent artery preservation, but the technical difficulty and significant morbidity have precluded its widespread use.[1] In 1974, Serbinenko reported his experience with detachable balloons for treating CCFs. [2] This technique results in closure of the fistula with ICA preservation in up to 80% of cases and has been the first-line therapy for direct CCFs.[3] Easy delivery and low cost are the main advantages of this technique. However, it also has some technical problems such as early detachment/deflation of the balloon or occasional rupture of the balloon stabbed by the bone fragments. [4] Detachable coils were used in 1992 by Guglielmi with the advantages of thrombogenicity, controllable deposit, radiopacity, and biocompatibility.[5] Dense packing of the cavernous sinus might cause nerve paralysis. Furthermore, the coils may protrude into the ICA and cause embolic events. Liquid embolic agents including n-butylcyanoacrylate and Onyx have also been used solely or in combination with coils in treating direct CCFs with favorable results.[6, 7] The potential of the embolic agent refluxing into the ICA or draining veins is the main disadvantage of this approach. [8]

Recently, covered stents for treating CCFs have been reported.[4, 9, 10] But all these covered stents were not initially for neurovascular use. As the first device designed exclusively for intracranial vascular defect, the Willis covered stent (MicroPort, Shanghai, China), was approved by the Chinese Food and Drug Administration in 2013. It is a balloon-expandable endoprosthesis composed of a bare stent and an expandable polytetrafluoroethylene membrane. Recently, it has been used for aneurysms[11] and arterial dissections[12] with satisfying results. However, its application for CCF is still limited.[9] In this study, we will explore the feasibility and safety of this stent in treating direct CCF.

Materials And Methods

Results

Patients’ information

Three females and 7 males were enrolled in this study. The average age was 28±2.556 years (18-45 years) and the average medical course was 33.6±17.39 days (2days-6months). Eight patients were treated for the first time and the other 2 had been treated previously elsewhere. The typical symptoms include chemosis, exophthalmos, intracranial bruit, and ocular movement disorder. Detailed information of these patients was summarized in table 1.

Immediate angiographic results

Willis covered stents were successfully delivered and released in 9 of the 10 patients, except for one case due to the tortuous ICA, for whom the parent artery was occluded with detachable balloons after an occlusion test. Immediate blockage of the abnormal shunt was achieved in 6 patients with one stent for each patient. Endoleak occurred in 3 patients. For one patient, repeated balloon inflation dramatically diminished the endoleak (Patient 10). For another patient, endoleak remained even after repeated balloon dilation and another stent deployment, and this patient got parent artery occlusion with balloons after an occlusion test. The blood flow was compensated by the anterior and posterior communicating artery (Patient 2). For the third patient, endoleak was sealed with coils through a pre-set microcatheter (Case 4, Fig 4, Patient 4).

Clinical and graphical follow-up results

Symptoms gradually relieved after the operation in all patients. Clinical follow-up 1 month after discharge showed disappear of chemosis and no new neurological deficits in all patients. Ocular motor disturbance disappeared in two patients (Patients 2 and 7) and relieved in another (Patient 4). Clinical follow-up 6 and 24 months after initial discharge showed no related neurological defects in all patients except for decreased visual acuity in patient 2 and slight oculomotor paralysis in patient 4.

Angiographic follow-up was available in 7 patients 6 to 10 months after initial discharge. Slight in-stent stenosis was found in 1 case (Patient 10) at six-month follow-up. In the patient with slight endoleak at discharge (Patient 10), the endoleak disappeared. For the two patients who received parent artery occlusion, DSA follow-up was not arranged for their silent symptoms. One patient (Patient 8) refused DSA follow-up for intact neurological function and economic burden.

Illustrative cases

Case-1 (Patient 1)

A 25 years old girl was transferred to our department for right chemosis for 7 days after a vehicle accident. She was diagnosed as right CCF by six-vessel angiography. The fistula was successfully repaired with 1 Willis covered stent. At one-month follow-up, the right chemosis disappeared with no new neurological deficits. Angiographic follow-up six months after discharge showed patency of the parent artery with no stenosis (Fig 1). Clinical follow-up 6 and 24 months after initial discharge showed no neurological deficit.

Case-2 (Patient 8)

A 31 years old man was admitted for right chemosis and intracranial bruit for 2 months. He had head trauma 2 months ago and was diagnosed as traumatic CCF. He received embolization with coils and Onyx-18 in a local hospital. The signs relieved just after operation but aggravated in the last 10 days before being transferred to our hospital. DSA confirmed recurrence of the CCF, and the fistula was repaired by a Willis covered stent. The bruit disappeared just immediately after the operation and the chemosis gradually relieved and disappeared at one-month follow-up after discharge (Fig 2). This patient refused DSA follow-up as the economic burden. Clinical follow-up at 6 and 24 months showed disappear of the signs, but decreased right visual acuity.

Case-3 (Patient 10)　

A 35 years old man, who suffered from severe head trauma and subsequent intracranial hematoma evacuation and decompressive craniectomy 1.5 months ago, came to our department for persistent left chemosis and exophthalmos. DSA confirmed a left high flow CCF. A slight endoleak was encountered even after repeated balloon inflation and a second stent deployment. His eye signs gradually diminished and completely disappeared at the one-month clinical follow-up. Angiographic follow-up showed disappear of the endoleak and slight in-stent stenosis (Fig 3). Clinical follow-up 6 and 24 months showed no neurological signs.

Case 4 (Patient 4)

A 21 years old man suffered from chemosis, exophthalmos, intracranial bruit and ocular movement disorder for 6 days after a vehicle accident. Diagnostic angiography confirmed right CCF. To eliminate the potential endoleak, a microcatheter was pre-set into the cavernous sinus through the fistula. After stent deployment and a second balloon dilation, the unexpected endoleak was sealed with 2 coils just near the fistula (Fig 4). His signs gradually relieved and completely resolved at one-month follow-up. He received angiographic follow-up in a local hospital but lost the imaging data. The copied in-hospital record described disappear of the fistula with no in-stent stenosis. Clinical follow-up 24 months after initial discharge was normal.

Discussion

Originally approved as a ‘bailout’ in the event of coronary artery rupture, covered stents could reconstruct the vessel defects immediately while preserving the parent artery. Willis is the first covered stent exclusively designed for intracranial vasculature. In this paper, we shared our experience of this device for treating direct CCFs.

Compared with traditional treatment modalities for CCFs with coils, Onyx, and balloons, covered stent has some advantages: high overall complete occlusion rate; a relatively simple and rapid procedure; no coil herniation into the parent artery; no mass effect, and no CCF recanalization and recurrence. Of these advantages, the high overall complete occlusion rate is the most important.[13] However, there are also some limitations for covered stent in repairing vascular defects. First, small perforating vessel sacrifice restricts its usage. Absence of important branches at the cavernous ICA provides the feasibility of covered stent for direct CCFs. Second, the tortuous ICA makes delivery of the stiff stent difficult. To overcome this difficulty, a strong supporting system is necessary.[14] We proposed an effective delivery system as described above, which was consisted of 8F guiding catheter, 5F Navien catheter, XT-27 microcatheter and an exchanging microwire in co-axis. In our series, all stent deliveries with this system were successfully. In patient 3, unavailability of the soft Navien catheter lead to stent delivery failure. These results proved the necessity and efficacy of our delivering system.

Defined as persistent perfusion of the space between the stent graft and parent vessel wall, [15] endoleak occurred in 38.89% cases immediately after covered stent deployment, [16] which was consistent with our cases (30%, 3/10). As major endoleak remained even after repeated balloon dilation and a second stent deployment, we had to sacrifice the ICA with balloons in patient 2. In patient 10 (Case 3, Fig. 3), endoleak diminished after re-dilation of the balloon and disappeared spontaneously at 6-month follow-up. In patient 4 (Case 4), the endoleak was sealed with two coils via a pre-set microcatheter (Fig. 4). As we knew, this is the first report to pre-set a microcatheter for unexpected endoleak after stent deployment. As a pre-set microcatheter may induce a gap between the arterial wall and the stent leading to persistent endoleak, it is more reasonable to deliver the microcatheter via the venous route. Oblate vessel wall, diameter variance of the covered vessel, sharp bone fracture that stabbing the stent membrane, vasospasm, and stent diameter mismatch may contribute to immediate endoleak.[16] Balloon re-dilation and additional stent deployment were reported to solve this complication, and slight endoleak might disappear spontaneously in follow-up.[15] The efficacy of these strategies was validated in patient 10 (Case 3, Fig. 3). In this patient, endoleak dramatically relieved after repeated balloon dilation, and the residual endoleak disappeared spontaneously at the 6-month angiographic follow-up. For patient 2, parent artery was sacrificed as persistent endoleak despite repeated balloon dilation and a second stent deployment.

In-stent stenosis was reported to occur in 18.0% and 20.9% patients after Willis stent implantation at 2 and 6 years follow-up. [16] In our series, in-stent stenosis was seen in 1 case at 6 month follow-up (10.0%, Case 3, Fig. 3). Smoking and stent angulation were predictors of late in-stent stenosis.[16] Repeated balloon dilation induced intima damage may contribute to the aggressive intima hyperplasia in this patient. Aspirin was prescribed and intermittent clinical follow-up was scheduled for him.

Recurrent or partially occluded CCF is always a nightmare for physicians, as delivery of the microcatheter may be extremely difficult. Under this condition, covered stent may serve as an alternative. In patient 8 (Fig. 2, Case 2), the inferior petrosal sinus had already been occluded in the initial operation and covered stent was selected as the salvage treatment. The fistula was occluded immediately after stent deployment.

Conclusions

In conclusion, our initial results indicated that Willis covered stent is feasible and efficient in treating direct CCFs. More cases are needed to further elucidate this issue.

Abbreviations

Declarations

Ethics approval and consent to participate

This study was approved by the ethics committee of Qilu Hospital and informed written consents were obtained from all patients or their guardians.

Consent for publication

Consent for publication was obtained from each patient before operation.

Availability of data and materials

The datasets used during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests

Funding

This study was supported by the China postdoctoral science foundation [grant NO. 2019M660714].

Author contributions

QL designed this study and wrote the manuscript; CQ, YW and WS contributed to data collection, GL and DW supervised this study. All authors read and approved the final manuscript

Acknowledgements

Not applicable

References

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Table

Table 1 patient information

Note: F: female; M: Male; ICA: internal carotid artery; DSA: digital subtraction angiography