Transarterial Onyx embolization of jugular foramen dural arteriovenous fistula with spinal venous drainage manifesting as myelopathy—a case report and review of the literature

Abstract

We report a rare case of jugular foramen dural arteriovenous fistula (DAVF) with spinal venous drainage. A 48-year-old woman suffered from progressive weakness of lower extremities and incontinence of urine and feces for 14 days. Magnetic resonance imaging (MRI) revealed a tortuous posterior medullary vein at C2–T2 and ischemic signal at C2–C4 of the spinal cord. Brain MRI revealed an abnormal high signal near the left jugular foramen. Digital subtraction angiography of the spinal vascular was negative, while brain angiography showed a left jugular foramen DAVF with spinal perimedullary venous drainage. The patient recovered completely soon after endovascular embolization with Onyx-18. Diagnosis of a DAVF presenting with myelopathy is challenging. Early diagnosis and treatment are essential for a favorable outcome.

Introduction

An intracranial dural arteriovenous fistula (DAVF) is an abnormal connection between dural arteries and leptomeningeal veins or venous sinuses.¹ DAVFs account for 15% of all intracranial arteriovenous malformations.² DAVFs with perimedullary venous drainage (Cognard type V) account for about 5% of all intracranial DAVFs.^3,4 This type of DAVF usually presents with progressive myelopathy and less frequently hemorrhage. Difficulty in diagnosing Cognard type V has been repeatedly reported.^1,5,6 Because of the rarity and nonspecific clinical presentation and imaging features, it is often underdiagnosed and leads to irreversible morbidity such as progressive spinal cord and brainstem symptoms. If the possibility of this diagnosis is considered and embolization is performed without delay, the patient outcome could be favorable. Otherwise, it may lead to permanent neurologic deficit.⁵

To our knowledge, Cognard type V DAVF located at the jugular foramen is rare. We report such a case to highlight the importance of timely diagnosis and management.

Case report

A 48-year-old woman was referred to our department with a main complaint of progressive urinary and fecal incontinence and lower extremity weakness for 14 days. Physical examination was unremarkable except for diminished strength in both lower extremities (Level IV). Blood routine and biochemical examination were normal. Initial cervical spine enhanced magnetic resonance imaging (MRI) (Figure 1) revealed a tortuous posterior spinal vein at C2–T2 (white arrows) of the medullary and ischemia manifestation at C2–C4 (black arrows) of the spinal cord. Brain MRI (Figure 2 and 3) revealed an abnormal high signal (arrows in Figure 2 and short arrow in Figure 3) near the left jugular foramen (long arrow in Figure 3). We performed myelography, which turned out to be negative. Then we performed digital subtraction angiography (DSA) (Figure 4) of the brain and discovered a left jugular foramen DAVF mainly supplied by the meningeal ascending pharyngeal artery (big black arrow) and dural branch of the left occipital artery (gray arrow). Venous drainage included the anterior (big white arrow) and posterior (small black arrow) spinal veins. The shunt is near the jugular foramen (small white arrow).

Figure 1.

Sagittal-enhanced T1-weighted magnetic resonance (MR) image of the cervical spine shows a tortuous posterior spinal vein at C2–T2 (white arrows) of the medullary, as well as an ischemia manifestation at C2–C4 (black arrows) of the spinal cord.

Figure 2.

Axial T1-weighted magnetic resonance (MR) image of the brain shows a high signal at the trailing edge of the apical petrous bone (arrows). This is the drainage vein with low blood velocity near the jugular foramen.

Figure 3.

Axial T2-weighted magnetic resonance (MR) image of the brain also shows a high signal (short arrow) at the posterior lateral margin of the jugular foramen (long arrow).

Figure 4.

Lateral review of the left external carotid artery angiography before embolization. Dural arteriovenous fistula (DAVF) supplied by the left ascending pharyngeal artery (big black arrow) and dural branch of the occipital artery (gray arrow) and drained by the anterior and posterior vein of the medullary. The small white arrow shows the shunt. The posterior medullary vein (small black arrow) is relatively more dilated than the anterior medullary vein (big white arrow).

We performed a transarterial approach endovascular embolization for the patient. Under general anesthesia, a 6 F sheath was placed in the right femoral artery. The guiding catheter was flushed via a pressure bag with saline containing 3000 U of heparin/l. The dural branch of the left occipital artery was super-selectively catheterized with a dimethyl-sulfoxide-compatible microcatheter (Marathon; ev3, Irvine, CA, USA) and the microcatheter tip was in the desired position (as near as possible to the fistula). We injected 0.6 ml of Onyx-18 (ev3, Irvine, CA, USA). The shunt, feeding pedicle and fistula were completely obliterated (Figure 5). The first day after the operation her symptoms were significantly relieved. The second day after the procedure all the symptoms disappeared and the patient was discharged. Follow-up by phone at three months confirmed the favorable outcome.

Figure 5.

Lateral review of left occipital artery angiography after embolization. As illustrated, the shunt is completely occluded.

Review of previous cases

We searched the PubMed database using the keywords “dural arteriovenous fistula” and “jugular foramen.” We found two articles describing DAVF located at the jugular foramen region and two cases are reported.^7,8 Both of the two cases are males ages 63 and 53 years old. One presented with subarachnoid hemorrhage (SAH), and transarterial embolization with N-butyl cyanoacrylate (NBCA) was performed. Follow-up confirmed complete occlusion and good prognosis. The other patient presented with a several-year history of right-sided pulsatile tinnitus. Surgical operation was performed. Postoperative angiography showed complete obliteration of the DAVF.

We searched the database using the keywords “dural arteriovenous fistula,” “spinal venous drainage,” “myelopathy” and “Onyx.” We found four articles^6,9–11 describing five cases of intracranial DAVFs with spinal venous drainage manifesting as myelopathy and embolized with Onyx. There are six cases in all, including our case (Table 1). Ages ranged from 18 to 76 years old (average 47.8 years old). Five cases (83.3%) presented as progressive paraparesis and three (50%) had bladder dysfunction. The location of the DAVFs mainly are tentorial (n = 2), transverse sigmoid (n = 1), foramen magnum (n = 1), posterior petrous ridge (n = 1) and jugular foramen (n = 1). Feeding arteries are the meningohypophyseal trunk (MHT), middle meningeal artery (MMA), posterior auricular artery (PAA), ascending pharyngeal artery (AphA) and occipital artery (OA). In five (83.3%) cases, the drainage vein included both anterior and posterior spinal veins. Five (83.3%) cases achieved complete occlusion and follow-up conformed to three 0 grade, two 1 grade and one 2 grade of the modified Rankin Scale score (mRS) grading system.

Table 1.

Onyx embolization of intracranial dural arteriovenous fistula with spinal venous drainage manifesting as myelopathy from the literature.

Case no.	Age/sex	Presentation	Location	Feeding artery	Drainage vein	Angiography result	Outcome (mRS)
16	18/M	Bladder dysfunction	Tentorial	Lt MHT, lt MMA	Anterior and posterior spinal veins	Complete	2
29	69/M	Bilateral lower extremity weakness	Tentorial	Lt MMA, lt OA and PAA	Anterior and posterior spinal veins	Complete	1
39	34/F	Bilateral extremity weakness	Transverse sigmoid	Lt OA	Anterior and posterior spinal veins	Complete	0
410	38/M	Progressive paraparesis and bladder dysfunction	Foramen magnum	Rt OA, rt AphA	Anterior and posterior spinal veins	Complete	0
511	76/M	Nausea, vomiting and progressive paraparesis	Posterior petrous ridge	Rt MMA, rt AphA	Anterior spinal vein	Incomplete	1
6 (present case)	52/F	Bilateral lower extremity weakness and incontinence of urine and feces	Left jugular foramen	Lt AphA, lt OA	Anterior and posterior spinal veins	Complete	0

M: male; F: female; Lt: left; Rt: right; MHT: meningohypophyseal trunk; MMA: middle meningeal artery; PAA: posterior auricular artery; AphA: ascending pharyngeal artery; OA: occipital artery; mRS: modified Rankin Scale score.

Discussion

Based on the pattern of venous drainage and its relationship with the surrounding cerebral venous, Cognard classified DAVFs into five categories. Cognard V DAVF, predominantly located in the posterior fossa around the tentorium and foramen magnum, was first reported as a cause of spinal myelopathy in 1982.^12–14 Because of its rarity, only a few cases have been reported. Haryu et al. reported three cases and reviewed 54 Cognard V DAVF cases from 1988 to 2014 (27 case reports), among which only 25 cases (20 males, five females) presented with only myelopathy.¹⁵ Wang et al. reviewed 127 craniocervical junction DAVF patients from 1970 to 2014; 46 (37.1%) presented with myelopathy and were mainly located at the tentorium, superior petrosal sinus, inferior petrosal sinus and transvers-sigmoid sinus.¹⁶ This report of type V DAVF located at the jugular foramen will enrich the clinical classification of this rare entity.

Diagnosis of an intracranial DAVF presenting only with myelopathy symptoms is usually challenging since early symptoms and imaging findings such as signal voids of the vessel are nonspecific. Sometimes it may be misdiagnosed as myelitis or degeneration diseases. Comprehensive spinal angiographic studies could not locate the DAVF; even bilateral vertebral angiography initially failed to demonstrate the fistula. In that case, cerebral angiography with catheterization of the internal carotid, external carotid, and vertebral arteries was the key to diagnosis.^6,17 In our case, T1-weighted image of MR (Figure 2) showed a high signal at the trailing edge of the apical petrous bone (arrows). A T2-weighted image (Figure 3) showed a high signal (short arrow) at the posterior lateral margin of the jugular foramen (long arrow). These abnormalities did not draw too much of our attention at first because these manifestations are not typical. Abnormal manifestations of the spine are more obvious. So we performed myelography based on the abnormality of MRI and clinical presentation, and the result turned out to be negative. Later cerebral angiography confirmed the lesion. Then we looked back at the MRI of the brain. We could understand why the abnormal signals near the left jugular foramen are all high signal. That may be because the blood flow rate in the drainage vein is too low to present as signal voids. Thus, when facing a patient presenting with myelopathy symptoms, abnormal MRI but normal spinal angiography, the practitioner should come up with an intracranial Cognard V DAVF located at craniocervical junction region or posterior fossa, and brain angiography is sometimes helpful and recommended.

DAVF with perimedullary vein drainage would cause chronic and progressive myelopathy symptoms. The drainage veins could be both anterior and posterior spinal veins. A direct shunt between the feeding pedicle and perimedullary vascular will lead to abnormal high pressure of the drainage vein, which would cause mass effect. In addition, normal venous drainage around the dilated vein will be obstructed and cause local venous congestion and consequently cord edema. All these pathophysiological changes could lead to local hypoxic-ischemic damage, including necrosis and apoptosis of nerve cells.¹⁸ Pathological changes may include some of the above changes as in our case. Image examination revealed local ischemia (C2–C4). We do not consider irreversible changes such as necrosis and apoptosis of nerve cells in our case considering the rapid recovery after embolization. Compression from the dilated posterior spinal vein lead to blocking of nerve conduction of the corticospinal tract and spinothalamic tract, which present as progressive weakness of the lower extremities and urinary and fecal incontinence. Endovascular therapy is a safe and effective method in the treatment of these fistulas and should be the first option.¹⁹ The purpose is direct closure of the shunt with a liquid embolic agent. Transarterial embolization is feasible and usually considered as the first choice.^17,20 Recently, the use of Onyx in DAVF embolization has been increasingly reported with promising results.²¹ In our case, a period of 14 days from the appearance of symptoms to presentation, combined with the prognosis, indicated that early diagnosis and treatment is extremely essential for preventing permanent nerve dysfunction.

In conclusion, this case of jugular foramen Cognard V DAVF enriched the clinical classification of this rare entity. Brain angiography is recommended for patients presenting with myelopathy symptoms, abnormal MRI but normal spinal angiography. Onyx embolization at the early stages is feasible and prognosis could be promising.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.