Percutaneous transjugular approach without arterial monitoring for the treatment of a direct carotid-cavernous fistula with vascular Ehlers–Danlos syndrome: illustrative case

Naoyuki Uchiyama Departments of Neurosurgery, Ishikawa Prefectural Central Hospital, Kanazawa, Ishikawa, Japan; and

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Yosuke Kawahara Departments of Neurosurgery, Ishikawa Prefectural Central Hospital, Kanazawa, Ishikawa, Japan; and

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Wataru Uchida Departments of Neurosurgery, Ishikawa Prefectural Central Hospital, Kanazawa, Ishikawa, Japan; and

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Ayumu Nitta Departments of Neurosurgery, Ishikawa Prefectural Central Hospital, Kanazawa, Ishikawa, Japan; and

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Atsushi Nohara Department of Clinical Genetics, Ishikawa Prefectural Central Hospital, Kanazawa, Ishikawa, Japan

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Yutaka Hayashi Departments of Neurosurgery, Ishikawa Prefectural Central Hospital, Kanazawa, Ishikawa, Japan; and

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BACKGROUND

Vascular Ehlers–Danlos syndrome (vEDS) because of COL3A1 mutations is a rare inherited collagen vascular disease associated with spontaneous arterial dissections, aneurysms, vessel rupture, and organ rupture. A direct carotid-cavernous fistula (CCF) is the most common central nervous system vascular anomaly in vEDS; however, its treatment is challenging due to extremely fragile arteries and veins.

OBSERVATIONS

A 22-year-old woman presented with pulsatile tinnitus and mild diplopia. CCF formation without trauma, cervical dissecting aneurysms, thin skin, and multiple ligament tears, as well as a genetic analysis, led to a diagnosis of vEDS. To minimize the risk of vascular injury in the thoracoperitoneal cavity, the internal jugular vein was directly punctured and the CCF was embolized transvenously using the triple-overlay road-mapping technique without arterial monitoring. The CCF was completely occluded, and the patient showed an excellent clinical course without neurological or vascular complications.

LESSONS

Physicians and neurosurgeons should consider vEDS when treating younger patients with spontaneous CCF without trauma and investigate the possibility of genetic abnormalities and systemic vascular pathology. Transvenous embolization of a CCF through the transjugular route using the triple-overlay road-mapping technique can minimize the risk of vascular injury in a patient with vEDS.

ABBREVIATIONS

CB = cone-beam; CCF = carotid-cavernous fistula; CS = cavernous sinus; CT = computed tomography; ICA = internal carotid artery; IPS = inferior petrosal sinus; MRA = magnetic resonance angiography; SMCV = superficial middle cerebral vein; SOV = superior ophthalmic vein; SPS = superior petrosal sinus; TVE = transvenous embolization; vEDS = vascular Ehlers–Danlos syndrome; 3D = three-dimensional

BACKGROUND

Vascular Ehlers–Danlos syndrome (vEDS) because of COL3A1 mutations is a rare inherited collagen vascular disease associated with spontaneous arterial dissections, aneurysms, vessel rupture, and organ rupture. A direct carotid-cavernous fistula (CCF) is the most common central nervous system vascular anomaly in vEDS; however, its treatment is challenging due to extremely fragile arteries and veins.

OBSERVATIONS

A 22-year-old woman presented with pulsatile tinnitus and mild diplopia. CCF formation without trauma, cervical dissecting aneurysms, thin skin, and multiple ligament tears, as well as a genetic analysis, led to a diagnosis of vEDS. To minimize the risk of vascular injury in the thoracoperitoneal cavity, the internal jugular vein was directly punctured and the CCF was embolized transvenously using the triple-overlay road-mapping technique without arterial monitoring. The CCF was completely occluded, and the patient showed an excellent clinical course without neurological or vascular complications.

LESSONS

Physicians and neurosurgeons should consider vEDS when treating younger patients with spontaneous CCF without trauma and investigate the possibility of genetic abnormalities and systemic vascular pathology. Transvenous embolization of a CCF through the transjugular route using the triple-overlay road-mapping technique can minimize the risk of vascular injury in a patient with vEDS.

ABBREVIATIONS

CB = cone-beam; CCF = carotid-cavernous fistula; CS = cavernous sinus; CT = computed tomography; ICA = internal carotid artery; IPS = inferior petrosal sinus; MRA = magnetic resonance angiography; SMCV = superficial middle cerebral vein; SOV = superior ophthalmic vein; SPS = superior petrosal sinus; TVE = transvenous embolization; vEDS = vascular Ehlers–Danlos syndrome; 3D = three-dimensional

A carotid-cavernous fistula (CCF) represents an abnormal connection between the carotid artery or its branches and the cavernous sinus (CS).1 CCFs can be classified according to their etiology (traumatic or spontaneous), blood flow velocity (high or low), and anatomy (direct or indirect). According to Barrow’s classification, there are four types of CCFs.1 A type A, or direct, CCF is a high-flow direct shunt caused by a posttraumatic or ruptured aneurysm, resulting in the short circuit of internal carotid artery (ICA) blood into the CS venous system. Types B, C, and D are low-flow lesions grouped together under the common definition of dural or indirect CCFs. Spontaneous direct CCFs grow in patients with intracavernous aneurysms and in patients with connective tissue diseases associated with vessel wall fragility, especially vascular Ehlers–Danlos syndrome (vEDS).2–5 Given that direct CCFs can cause progressive deterioration of visual acuity and intracranial hemorrhage due to ophthalmic and cortical venous reflux, treatment to stop shunt flow is imperative. The treatment of direct CCFs in patients with vEDS is particularly challenging. In these patients, even conventional catheter diagnostic angiography can result in large artery dissection and vessel rupture.6 The treatment of direct CCFs in vEDS is accompanied by a mortality rate of up to 59% after initial treatment, 23% of which is directly related to therapy.6

In this report, we present the case of a patient with vEDS who developed a spontaneous direct CCF resulting from aneurysm rupture. After confirmation of the genetic diagnosis of vEDS, the direct CCF was treated with transvenous embolization (TVE) via a directly punctured internal jugular vein using the triple-overlay road-mapping technique7,8 without arterial access. To the best of our knowledge, this novel approach has not been used in the management of CCFs in patients with vEDS to date.

Illustrative Case

History and Examination

A 22-year-old woman was referred to our hospital with a 7-month history of new-onset left-sided pulsatile tinnitus and a 2-month history of mild diplopia with extreme horizontal left gaze. The patient had no history of head trauma. She had experienced three anterior cruciate ligament tears while playing basketball and had undergone reconstructive surgeries when she was 9, 11, and 13 years of age. Her family history was unremarkable. Physical examination revealed mild left abducens nerve palsy and a pulsatile bruit in the left orbit. No proptosis, conjunctival chemosis, or decreased visual acuity was observed (Fig. 1A and B). Although magnetic resonance imaging of the brain revealed a CCF on the left side (Fig. 1C and D), it was not clear whether the CCF was direct or indirect. At this point, we were unaware of the existence of any collagen vascular diseases such as vEDS.

FIG. 1.
FIG. 1.

Photographs showing mild abduction restriction of the left eye with no proptosis or conjunctival chemosis at the time of presentation to our hospital (A and B). Magnetic resonance angiography (MRA) showing the cavernous sinus (CS; arrows), superior petrosal sinus (SPS; double arrows), and inferior petrosal sinus (IPS; triple arrows) as an indication of a carotid-cavernous fistula (CCF): time-of-flight image (C) and source image (D).

Cerebral angiography was performed via the transfemoral route. An 11-cm 4-Fr sheath (Terumo) was inserted into the right femoral artery, and a 100-cm 4-Fr diagnostic catheter (Berenstein type, Terumo) with a 220-cm 0.035-inch guidewire (Terumo) was used. Left carotid angiograms confirmed a direct CCF (Fig. 2). Three-dimensional (3D) rotational angiography clearly showed a fistula between the aneurysm of the cavernous portion of the ICA and CS (Fig. 2E). Draining proceeded via the superior petrosal sinus (SPS) and inferior petrosal sinus (IPS; Fig. 2B and D). Drainage flow to the SPS was refluxed into the petrous vein, with retrograde filling of several cortical cerebellar veins (Fig. 2B). No drainage flow into the superior ophthalmic vein (SOV) or superficial middle cerebral vein (SMCV) was observed. Right carotid angiograms revealed dissecting aneurysms of the external carotid artery and the cervical ICA (Fig. 2C). Bilateral vertebral angiography showed no abnormal findings. After angiography, we noticed thin, translucent skin on her anterior chest with increased venous visibility. Direct CCF formation without trauma, dissecting aneurysms of the cervical carotid artery, thin skin, and multiple ligament tears led us to strongly suspect a vEDS phenotype. Fortunately, 3D computed tomography (CT) angiography, which was performed 3 days after the angiography, did not show any intimal tears in the major blood vessels or dissections of the iliac, femoral, and carotid arteries (Fig. 3). We consulted a physician at the Department of Clinical Genetics and requested a genetic analysis and counseling for her family. The genetic analysis revealed a COL3A1 mutation (c.3284G > T, p.Gly1095Val), confirming the diagnosis of vEDS. The patient and her family were sufficiently informed of the high risk of arterial catheterization in vEDS, and conservative therapy with celiprolol, which has been reported to reduce vascular complications in patients with vEDS, was initiated at 100 mg per day. Since the patient’s pulsatile tinnitus and left abducens nerve palsy gradually worsened in the following 6 weeks, endovascular treatment was subsequently planned.

FIG. 2.
FIG. 2.

Left common carotid artery (CCA) angiogram (A), anteroposterior view, showing a left CCF. Left CCA angiogram (B), lateral view, showing drainage flow to the SPS (arrow) refluxing into the petrous vein with retrograde filling of the cortical cerebellar veins (double arrows). Right CCA angiogram (C), anteroposterior view, showing dissecting aneurysms of the cervical internal carotid (arrow) and external carotid (double arrows) arteries. Left CCA angiogram (D), anteroinferior oblique view, showing the internal carotid artery (ICA; arrowhead), the CS (arrow) with a drainage route to the SPS (double arrows) and IPS (triple arrows). Three-dimensional (3D) rotational angiogram (E) showing a fistula (arrows) between an aneurysm (double arrowheads) on the ICA (single arrowhead) and CS.

FIG. 3.
FIG. 3.

3D computed tomography (CT) angiography showing no dissections of the aorta (A) and iliac and femoral arteries (B).

Treatment

The procedure was performed with the patient under general anesthesia in a biplane neurointerventional suite using an Azurion Xper FD 20/15 angiographic unit and XtraVision workstation (Philips Medical Systems). Systemic heparinization was not performed because no catheter was placed on the arterial side. We used triple-overlay road-mapping, which was previously described by Levitt et al.7 and Huynh et al.8 Briefly, preintervention magnetic resonance angiography (MRA) data were imported to the XtraVision workstation and co-registered with the cone-beam (CB) CT data, which was performed using the Azurion system on the day of the intervention. This allowed the blood vessels from both volumetric data sets to be overlaid using live fluoroscopy from any viewing angle and using any gantry configuration.

We then cannulated the left internal jugular vein using ultrasound guidance as well as the triple-overlay road-mapping technique and placed a 90-cm 6-Fr Fubuki guiding catheter (ASAHI Intecc) percutaneously. One microcatheter (Headway 17, Terumo) was advanced into the SPS, and the other (Headway 21, Terumo) was advanced into the shunt segment (i.e., the anterior compartment of the CS) just downstream of the shunting point. Navigation of the microcatheters and microguidewires was performed via the IPS using the triple-overlay information from MRA, CB CT, and live fluoroscopy to outline the IPS, SPS, and CS (Video 1).

VIDEO 1. Clip showing canulation of the internal jugular vein and navigation of the microcatheter and microguidewires to the superior petrosal sinus (SPS) and cavernous sinus (CS) via the inferior petrosal sinus (IPS) using the triple-overlay road-mapping technique. Click here to view.

Ten hydrocoils (Terumo) were then deployed through the Headway 17 microcatheter within the SPS to stop venous reflux into the cerebellar vein, and occlusion was confirmed with an injection from the Headway 21 microcatheter in the CS (Video 2). Subsequently, an additional 10 hydrocoils were deployed near the fistula in the CS through the Headway 21 microcatheter. The final microcatheter injection revealed stagnation of the contrast medium within the CS and IPS, indicating fistula occlusion (Fig. 4A and B). Intravenous digital subtraction angiography, which was performed by infusing 50 mL of contrast through the Fubuki guiding catheter, confirmed the complete obliteration of the fistula (Fig. 4C and D). The Fubuki catheter was removed, and hemostasis was achieved by manual compression. The patient was admitted to the intensive care unit and kept sedated and ventilated, and strict blood pressure control was maintained for 3 hours. After confirming the absence of subcutaneous hematoma at the puncture site, the patient was extubated.

VIDEO 2. Clip showing coil embolization of the SPS and CS, stasis of contrast in the CS and IPS, and intravenous digital subtraction angiography. Click here to view.

FIG. 4.
FIG. 4.

Anteroposterior (A) and lateral (B) final microcatheter injection of the left CS in the late phase showing the stasis of contrast in the CS and IPS without ophthalmic or cortical vein opacification, suggesting occlusion of the CCF. Anteroposterior (C) and lateral (D) final postembolization intravenous digital subtraction angiograms confirm complete occlusion of the left direct CCF without evidence of early venous drainage.

MRA performed on the following day showed occlusion of the fistula (Fig. 5A and B), and 3D CT angiography performed 5 days later showed neither venous aneurysm formation nor occlusion of the internal jugular vein at the puncture site (Fig. 5C and D). The patient was discharged on postprocedural day 7 with complete resolution of the pulsatile tinnitus and significant improvement in left extraocular movements.

FIG. 5.
FIG. 5.

Postoperative day 1 MRA showing occlusion of the left CCF (A). The source image (B) of the MRA showing that the coil compartment around the left ICA is of a very low intensity signal (arrows) and that the shunt is occluded. Photograph (C) on postoperative day 5 showing a small scar without subcutaneous hematoma at the puncture site. 3D CT angiography (D) on postoperative day 5 demonstrates no formation of a venous aneurysm.

Posttreatment Course

At the 3-month follow-up, the abducens nerve palsy was completely cured and MRA demonstrated no recurrence of CCFs. Moreover, no treatment had to be administered, as the right external carotid artery and cervical ICA were asymptomatic and demonstrated no change in size or shape.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Vascular Ehlers–Danlos syndrome, the least common form of EDS, has an estimated prevalence of 1 in 150,000 persons.9 Arterial fragility results from mutations in COL3A1, which encodes type III collagen, leading to life-threatening features including arterial dissections, gastrointestinal perforations, spontaneous arterial ruptures, and uterine ruptures.9 It is a known pathogenic factor for the development of intracranial and extracranial vascular abnormalities, which may induce major neurological complications such as CCFs, aneurysms of the circle of Willis, and postarteriographic vascular blowouts.10

Observations

In one retrospective study, the median age of patients at diagnosis was 29 years.11 The median survival is reported to be 40–50 years, with the first complication usually observed by the age of 20 years.12 Therefore, this is a crucial diagnosis. Even for experienced clinicians, however, the clinical diagnosis of vEDS is difficult because of the potential lack of classic signs and symptoms of hypermobility in vEDS. It is imperative that the patient’s history is revisited to identify overlooked signs and symptoms, such as thin translucent skin, easy bruising, or tendon and muscle ruptures. Spontaneous CCFs associated with vEDS have also been previously reported. One case series reported that 3% of cases (6/202) had CCFs.3 Recently, Adham et al.13 identified 13 (9.8%) individuals with direct CCFs among 133 patients with molecularly diagnosed vEDS. Nine (69%) of these patients experienced direct CCFs as their first vascular event. Notably, direct CCFs were recently included as a major diagnostic criterion in the 2017 classification of vEDS,14 although in 1997, it was classified as a minor criterion.4 In younger patients with spontaneous CCFs without trauma, physicians and neurosurgeons should suspect vEDS and investigate the genetic abnormality because the natural course of vEDS is impacted by the type of COL3A1 mutation. More severe clinical and phenotypical presentations are attributable to glycine missense and splice-site variants rather than variants leading to haploinsufficiency.9 After confirmation of a genetic diagnosis, the systemic vascular pathology should be evaluated using noninvasive methods such as CT/MRA for appropriate prophylactic measures. Only one clinical trial of a potential drug therapy to prevent vascular events in patients with vEDS has been published.12 This trial showed that celiprolol, a cardioselective β-blocker, decreased the vascular complication rate by three-fold in patients with vEDS.

Endovascular treatment is considered the primary treatment for CCFs. Transarterial balloon embolization has been commonly used in the management of direct CCFs.15,16 Alternatively, platinum coil embolization via transarterial or transvenous routes has emerged as a promising method because coils can be easily deployed, controlled, and retrieved.17 However, in vEDS, the fragility of the blood vessels means that standard endovascular interventions are very hazardous. Schievink et al.6 reviewed 17 cases of direct CCFs with vEDS that had been reported prior to 1991. They documented a 35% morbidity rate, 12% mortality rate with diagnostic angiography, and 17% death rate resulting from interventional therapy. As the high complication rate is often due to arterial rupture, working from the venous side of the fistula is considered safer when attempting occlusion in these patients.18,19 However, despite TVE, remote vascular complications including hemothorax, abdominal aortic and cardiac ruptures, and iliac artery perforation have been reported.20,21 Most of these can be attributed to transfemoral arterial access for the placement of a monitoring catheter in the carotid artery. To prevent arterial wall injury, Van Overmeire et al.22 reported pure TVE for a direct CCF in a patient with vEDS without arterial puncture for monitoring purposes intraoperatively; however, 10 days after treatment, the patient died because of intraperitoneal hemorrhage, probably due to the rupture of a large-caliber vein on the transfemoral route. These reports have shown that the transfemoral approach, whether arterial or venous, can cause fatal bleeding in the thoracoperitoneal cavity.

To avoid the risks associated with the transfemoral approach, several authors have recommended surgical exposure of the ipsilateral carotid artery and internal jugular vein with the placement of endovascular sheaths.23–25 However, carotid artery puncture carries the risk of carotid dissection and/or aneurysm formation. By using the triple-overlay road-mapping technique, we could safely omit arterial access and puncture the jugular vein. Hemostasis can be achieved via manual compression with postoperative sedation and strict blood pressure control within a few hours. We believe that the transjugular approach from the neck without arterial access would be an ideal method to minimize the risk of vascular complications in the treatment of direct CCFs associated with vEDS. To the best of our knowledge, this is the first report of a percutaneous transjugular approach for the management of a CCF in a patient with vEDS to date.

As the IPS, SPS, and CS of our patient were distinctly depicted using the preprocedural MRA, these venous sinuses were clearly shown on the 3D roadmap. Since the 3D roadmap might be offset by a few millimeters, microinjection was necessary to confirm the accurate position of microcatheters. Despite this, because it was easy to clearly visualize the angle between the ICA and CS, we could still confirm whether the coil(s) had deviated into the carotid artery side when embolizing near the fistula, thereby minimizing overlaying errors. The concern is the change in the drainage route.26,27 As the outflow channel becomes occluded, a new drainage route that induces venous hypertension and subsequent cerebral hemorrhage may appear. Usually, this change can be immediately confirmed by injection from a monitoring catheter in the carotid artery. A microcatheter near the fistula can be a substitute in the absence of a monitoring catheter. Therefore, we recommend the insertion of a double microcatheter. This time, we first embolized the SPS to stop the dangerous drainage to the posterior fossa. Microcatheter injection near the fistula in the CS confirmed that drainage to the posterior fossa had stopped and that no other drainage routes, such as the SOV or SMCV, had emerged. Additionally, occlusion of the CCF can be determined by stasis of the contrast from the microcatheter injection in the CS and IPS. The insertion of double microcatheters is valuable for determining the change in the drainage route and the status of embolization without a monitoring catheter.

Lessons

When seeing a younger patient with a spontaneous CCF without trauma, physicians and neurosurgeons should suspect vEDS and investigate the possibility of genetic abnormalities and a systemic vascular pathology. Treatment of direct CCFs in patients with vEDS is possible, but the risk of complications due to vessel fragility is high. TVE of CCFs through the percutaneous transjugular route using the triple-overlay road-mapping technique without arterial access can minimize the risk of vascular injuries in a patient with vEDS.

Acknowledgments

We express our special thanks to Prof. Tomoki Kosho from the Department of Medical Genetics of Shinshu University School of Medicine for his insightful suggestions and comments.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Uchiyama, Uchida, Nitta. Acquisition of data: Uchiyama, Nohara. Analysis and interpretation of data: Uchiyama, Nohara. Drafting of the article: Uchiyama, Nohara. Critically revising the article: Uchiyama, Kawahara, Nohara, Hayashi. Reviewed submitted version of the manuscript: Uchiyama, Kawahara, Nohara. Approved the final version of the manuscript on behalf of all authors: Uchiyama. Administrative/technical/material support: Uchiyama. Study supervision: Hayashi.

Supplemental Information

References

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  • FIG. 1.

    Photographs showing mild abduction restriction of the left eye with no proptosis or conjunctival chemosis at the time of presentation to our hospital (A and B). Magnetic resonance angiography (MRA) showing the cavernous sinus (CS; arrows), superior petrosal sinus (SPS; double arrows), and inferior petrosal sinus (IPS; triple arrows) as an indication of a carotid-cavernous fistula (CCF): time-of-flight image (C) and source image (D).

  • FIG. 2.

    Left common carotid artery (CCA) angiogram (A), anteroposterior view, showing a left CCF. Left CCA angiogram (B), lateral view, showing drainage flow to the SPS (arrow) refluxing into the petrous vein with retrograde filling of the cortical cerebellar veins (double arrows). Right CCA angiogram (C), anteroposterior view, showing dissecting aneurysms of the cervical internal carotid (arrow) and external carotid (double arrows) arteries. Left CCA angiogram (D), anteroinferior oblique view, showing the internal carotid artery (ICA; arrowhead), the CS (arrow) with a drainage route to the SPS (double arrows) and IPS (triple arrows). Three-dimensional (3D) rotational angiogram (E) showing a fistula (arrows) between an aneurysm (double arrowheads) on the ICA (single arrowhead) and CS.

  • FIG. 3.

    3D computed tomography (CT) angiography showing no dissections of the aorta (A) and iliac and femoral arteries (B).

  • FIG. 4.

    Anteroposterior (A) and lateral (B) final microcatheter injection of the left CS in the late phase showing the stasis of contrast in the CS and IPS without ophthalmic or cortical vein opacification, suggesting occlusion of the CCF. Anteroposterior (C) and lateral (D) final postembolization intravenous digital subtraction angiograms confirm complete occlusion of the left direct CCF without evidence of early venous drainage.

  • FIG. 5.

    Postoperative day 1 MRA showing occlusion of the left CCF (A). The source image (B) of the MRA showing that the coil compartment around the left ICA is of a very low intensity signal (arrows) and that the shunt is occluded. Photograph (C) on postoperative day 5 showing a small scar without subcutaneous hematoma at the puncture site. 3D CT angiography (D) on postoperative day 5 demonstrates no formation of a venous aneurysm.

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