Tentorial Dural Arteriovenous Fistula Presenting with Quadriparesis: Case Report and Review of the Literature

Tentorial Dural Arteriovenous Fistula Presenting with Quadriparesis: Case Report and Review of the Literature Sara Khan, MD, David W. Polston, MD, Robert W. Shields Jr, MD, Peter Rasmussen, MD, and Rishi Gupta, MD

Tentorial dural arteriovenous fistulas (TDAVFs) draining into the spinal venous system are rare lesions. The clinical presentation can be devastating and the diagnosis delayed because of the initial nonspecific imaging and laboratory findings. We report a case of a 20-year-old woman with a rapidly progressive myelopathy, who was found to have a left TDAVF, fed by a single arterial feeder with drainage into the perimedullary venous system. The fistula was surgically clipped. The patient showed neurologic improvement at her 3-month follow-up but still had significant weakness of all 4 extremities. Early diagnosis is key as the neurologic symptoms are reversible with appropriate treatment. We review the relevant literature, imaging characteristics, and treatment modalities for TDAVF. Key Words: Tentorial dural arteriovenous fistula—myelopathy—perimedullary venous drainage—magnetic resonance imaging. Ó 2009 by National Stroke Association

Intracranial vascular malformations are a well-recognized entity that can present with a broad spectrum of neurologic signs and symptoms. Dural arteriovenous fistula (DAVF) constitutes 10% to 15% of these malformations.1-3 All fistulas have one or more feeding arteries, derived from the dural arteries or meningeal branches of cerebral arteries, with venous drainage into a venous sinus, eptomeningeal, or spinal veins.1,4,5 Meningeal arteries penetrate the dura through a venous sinus, on their way to supply the brain and spinal cord.5 This close proximity between the meningeal arteries and the venous sinuses predisposes to the development of a fistula.5 In tentorial DAVF (TDAVF), the fistula resides within the dura that constitutes the wall of the tentorial sinus.3 TDAVFs account for 8.4% of intracranial DAVFs.1 These are known to be aggressive vascular lesions, as the shunt

From the Cleveland Clinic Foundation, Ohio. Received August 28, 2008; revision received December 15, 2008; accepted December 29, 2008. Address correspondence to Rishi Gupta, MD, The Cleveland Clinic Foundation, 9500 Euclid Ave, S80, Cleveland, OH 44195. E-mail: [email protected]. 1052-3057/$—see front matter Ó 2009 by National Stroke Association doi:10.1016/j.jstrokecerebrovasdis.2008.12.007

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often results in obliteration of the tentorial sinus with associated cortical venous reflux or involvement of the perimedullary venous plexus.1,2,6 We present a young patient with a TDAVF with spinal venous drainage, presenting with rapidly progressive neurologic symptoms secondary to brainstem and cervical cord edema.

Case Report A 20-year-old woman presented with a 2-week history of neurologic symptoms. The symptoms began with bilateral leg pain and tingling, with ascending numbness during the course of a few days. Four days after symptom onset, she noticed leg weakness with progressive difficulty in walking along with intractable vomiting and constipation. A week later she developed urinary retention and at this point was admitted to an outside hospital. Her symptoms continued to progress and at the time of admission to our hospital she was unable to move her lower extremities, developed weakness of her right upper extremity, and had dysphagia and difficulty breathing. She was intubated for respiratory distress 2 weeks after symptom onset. On admission the patient was alert and oriented. Cranial nerves were intact. Motor examination revealed

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Figure 1. MRI: T2-weighted images, revealing confluent hyperintensity from caudal aspect of pons to upper cervical spinal cord (C3). Typical central venous edema pattern extending to periphery with prominent veins in pontine tegmentum and along margins of cervicomedullary junction.

generalized hypotonia. She demonstrated no movement in her lower extremities and was able to move both her upper extremities against gravity but not against resistance. Reflexes were absent in the lower extremities and normal in the upper extremities. A positive Babinski’s sign was observed on the left. There was decreased sensation to all modalities in both lower extremities, right more then left, and loss of sensation in the right arm and face to touch and pin prick. She was using her accessory muscles of respiration. The patient progressed to flaccid quadriplegia 2 days after admission. Magnetic resonance imaging (MRI) of brain and spinal cord revealed a confluent hyperintensity on fluid-attenuated inversion recovery and T2-weighted images, extending from the caudal pons to C3 vertebral level (Fig 1). No contrast enhancement was observed. Cerebrospinal fluid (CSF) analysis showed an elevated white blood cell count of 11 u/L and an elevated IgG index. The rest of the CSF studies including glucose, protein, myelin basic protein, oligoclonal bands, cytology, and angiotensin-converting enzyme levels were within normal limits. CSF and blood findings were negative for a viral, fungal, or bacterial source. Angiotensin-converting enzyme levels in blood were normal. Neuromyelitis optica was suggested, but

antibodies against aquaporin-4 were negative. Based on the MRI findings and an elevated IgG index, a demyelinating process was suspected and high-dose steroids were started followed by plasmapheresis, with minimal improvement of symptoms. A repeat MRI was performed 2 weeks later and showed extension of the lesion, now with increased vascularity around and within the involved brainstem (Fig 2). A complete cerebral angiogram was performed including subselective injections of the external carotid arteries, ascending pharyngeal arteries, occipital arteries, and thyrocervical trunks. The angiogram revealed a DAVF along the left tentorium. This was fed by a single feeder, the tentorial artery of Bernasconi and Cassinari, with associated engorgement of the cerebellar veins and the anterior spinal vein (not shown) (Fig 3, A and B). The patient underwent successful surgical clipping of the TDAVF, with postoperative angiogram showing obliteration of the fistula (Fig 3, C). Postoperatively, the patient showed improvement in her left arm strength with some antigravity movement of the forearm. There was no movement of her lower extremities. The patient was discharged after a tracheostomy and perutaneous endoscopic gastrostomy (PEG)

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Figure 2. MRI T2-weighted images 2 weeks later. Extension of edema into dorsal pons. There was no enhancement on postcontrast images (not shown). Notice increased vascularity along and within involved brainstem and upper cervical cord.

tube placement. At 3-month follow-up, she was off the ventilator and had resolution of her dysphagia. She was able to move her arms against gravity but not against resistance and had significant weakness of her lower extremities. A follow-up angiogram at 3 months revealed persistent obliteration of the fistula and MRI showed interval resolution of brainstem and cervical cord edema (Fig 4). It is important to note that the patient’s clinical examination did not correlate to the significant improvement noted on neuroimaging.

Discussion A combination of diffuse signal change in the brainstem and spinal cord, with dilated perimedullary veins, presenting with a progressive myelopathy has been reported with TDAVFs with spinal venous drainage (Tables 1 and 2). However, the blood vessels can be difficult to identify on imaging, causing a significant delay in diagnosis. Clinical presentation and neuroimaging findings encompass a broad differential diagnosis, and may result in diagnostic and critical therapeutic delay. TDAVFs, as a whole, lack specific characteristics in their clinical presentation. Cranial nerve involvement,

headache, ataxia, trigeminal neuralgia, and acute hemorrhage have all been reported at presentation.1,3,7,8 The signs and symptoms in turn depend on the type of venous drainage. The classification of intracranial DAVFs has evolved over time, based on their venous drainage, natural history, and arterial feeders.2,4,5,9-11 Cognard et al4 classified DAVF into 5 types, on the basis of the pattern of venous drainage: type I, located in the main sinus, with anterograde flow; type II, in the main sinus, with reflux into the sinus (IIa), cortical veins (IIb), or both (IIa1b); type III, with direct cortical venous drainage without venous ectasia; type IV, with cortical venous drainage with venous ectasia; and type V, with spinal venous drainage. From their analysis of 205 patients, types III and IV DAVFs were associated with the highest risk of hemorrhage and type V was associated with a high risk of myelopathy (50%).4 Similarly, Borden et al5 also categorized DAVFs according to their venous drainage: type 1 with drainage directly into a dural venous sinus or meningeal vein with anterograde flow; type 2 with drainage into a venous sinus with retrograde flow into the subarachnoid veins; and type 3 with drainage into subarachnoid veins.5 Both types 2 and 3 DAVFs were associated with a higher incidence of hemorrhage and progressive neurologic deficit.

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Figure 3. Selective angiography of left internal carotid artery demonstrating tentorial dural arteriovenous fistula (arrow) fed by tentorial artery of Bernasconi and Cassinari, with drainage into cerebellar veins with tentorial sinus not visualized (arrowheads) (A). Postoperative angiogram with successful surgical clipping (arrow) of tentorial artery (B). Selective angiogram of left internal carotid artery after surgery, with obliteration of fistula (C).

Lawton et al12 specifically classified TDAVFs into 6 types based on their location, dural base, associated venous sinus, and venous drainage (as per the classification of Borden et al5), which in turn determined the surgical approach. According to their classification TDAVFs were divided into galenic, straight sinus, torcular, tentorial sinus, superior petrosal sinus, and incisural fistulas.12 Most recently, Geibprasert et al11 classified DAVFs into 3 categories, based on the association of the epidural venous spaces with the afferent veins from the surrounding calvarium and the central nervous system, according to their embryological development. These were the ventral, dorsal, and lateral epidural shunts.11 Per this classification, TDAVF would fall into the category of lateral epidural shunts, which were found to be more aggressive and associated with a higher risk of neurologic complications.11 TDAVFs are known to be aggressive lesions as a result of their leptomeningeal venous drainage pattern and the associated high risk of hemorrhage.1,3,4,10,11,13 Other reports have demonstrated TDAVFs manifesting with

myelopathy because of spinal venous drainage (Tables 1 and 2). Our patient presented with a rapidly progressive myelopathy with no evidence of subarachnoid or intraparenchymal hemorrhage. The severity of symptoms was caused by diffuse brainstem and cervical cord edema. This is attributed to the drainage of her TDAVF by spinal as opposed to leptomeningeal veins, resulting in persistent venous hypertension and congestion.14 Also unique about our patient was the fact that she developed symptoms at an age much younger then that previously reported.1,3,13 The origin of DAVFs is not entirely clear but they are largely considered to be acquired lesions. Trauma, surgery, sinus thrombosis, and congenital factors have been postulated as possible causes.1-3,13,15 Neuroimaging plays an important role in diagnosis. Dilated veins can be identified in the region of the tentorium signifying venous congestion. Edema as a result of increased venous pressure manifests as hyperintensity on fluid-attenuated inversion recovery and T2-weighted images, which may be seen in the brainstem, rostral

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Figure 4.

MRI T2-weighted images, 3 months postoperatively. Resolution of hyperintensity previously noticed in brainstem and cervical spinal cord.

Table 1. Clinical summary of selected reported cases of tentorial dural arteriovenous fistulas Author

No.of cases

Average age (y)

Clinical presentation

Average time to diagnosis

Wrobel et al21

3

51

Years

Awad et al1

4

47.5

Bret et al22

1

31

Brunereau et al9

5

55

Bousson et al23

1

36

Ricolfi et al19

2

61

Renner et al24

1

58

Wiesmann et al6

1

46

Leg weakness, sensory loss, paraparesis Hemorrhage or nonhemorrhagic brainstem symptoms Paraparesis, paresthesias, bladder dysfunction SAH, IVH, tetraparesis/ paraparesis Numbness in all extremities, tetraparesis Tetraparesis/paraparesis, sphincter dysfunction Sensory level, weakness, urinary incontinence HA, nausea, vomiting, ataxia, paraplegia

Zhou et al3

5

38

SAH, cranial nerve palsies, HA

Abbreviations: HA, headache; IVH, intraventricular hemorrhage; SAH, subarachnoid hemorrhage.

1-2 y

4 mo 4 mo Few mo to 3 y Few days

9.8 mo

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Table 2. Angiographic findings of reported cases of tentorial dural arteriovenous fistulas presenting with myelopathy Author Wrobel et al21

Awad et al1

Arterial supply

Venous drainage

Treatment

- OA, TA - OA, TA - MHT, OA, pharyngeal arteries - Lt OA and TA

- Petrosal, spinal veins - Petrosal, spinal veins - Spinal veins

Embolization, surgery Surgery Surgery

- Galenic drainage, sigmoid sinus occlusion - Galenic, prepontine veins - Galenic, large venous aneurysm - Galenic, prepontine variceal drainage - Rt transverse sinus, spinal veins - Perimesencephalic, spinal - Perimesencephalic, spinal - Perimesencephalic, spinal - Perimesencephalic, spinal - Perimesencephalic, spinal - Perimedullary veins - Pontomesencephalic vein

Embolization

- Ipsilateral OA and TA - Rt PCA, SCA, TA and ECA branches - Lt TA and ECA branches Bret et al22 Brunereau et al9

Bousson et al23 Ricolfi et al19

Renner et al24 Wiesmann et al6 Zhou et al3

- Rt MHT - Rt MMA, MHT - Lt MHT - Rt MMA - Lt MHT - Lt MHT - Lt OA - Lt artery of foramen rotundum, TA - Lt MMA, TA - Rt MHT - L MHT - MHT, MMA, SCA - MHT, MMA - MHT, MMA, PMA, PCA - MMA, PMA, PCA, SCA, OA - MHT, MMA, PCA, OA, PMA

- Pontomesencephalic, Petrosal vein of Dandy - Cervical and upper thoracic plexus - Perimesencephalic, spinal - Galenic and mesencephalic vein - Galenic, mesencephalic, spinal veins - Galenic and mesencephalic veins - Cerebellar veins - Leptomeningeal, perimesencephalic

Embolization, surgery Surgery Surgery Surgery Embolization Embolization Embolization, surgery Embolization, surgery Embolization Embolization, surgery Surgery Embolization, surgery Embolization, surgery Surgery

Abbreviations: ECA, external carotid artery; Lt, left; MHT, meningohypophyseal trunk branches; MMA, middle meningeal artery branches; OA, occipital artery; PCA, posterior cerebral artery; PMA, posterior meningeal artery; Rt, right; SCA, superior cerebellar artery branches; TA, tentorial artery.

cervical cord, cerebellum, and thalamus.3 If no vascular anomaly is identified, the differential diagnosis is broad, and includes demyelinating conditions, tumors, brainstem encephalitis, and vasculitis, to name a few. Ideally, in a patient with a rapidly progressive course, with normal CSF findings and the above-mentioned MRI findings, who are unresponsive to steroids, a venous cause of symptoms should be strongly considered. Cerebral angiography is the gold standard of diagnosis. Arterial feeders to TDAVFs are usually multiple and originate from the occipital artery, posterior meningeal artery, marginal tentorial artery, middle meningeal artery, meningeal branches of pial arteries, and branches of the external carotid artery.3,12,13,16 The tentorial artery, or the artery of Bernasconi and Cassinari, arises from branches of the in-

ternal carotid artery, most often the meningohypophyseal trunk.12 With the possibility of multiple arterial feeders of TDAVFs, every patient should be evaluated with bilateral internal and external carotid and vertebral angiography.15 The optimal management strategy for TDAVF is still controversial. In this particular patient, consideration can be given to direct catheterization of the marginal tentorial artery, but it was thought that the vessel was quite tortuous precluding placement of a microcatheter in a stable position for safe injection of a liquid embolic agent. A second option considered was inflation of a balloon distal to the marginal tentorial artery and infusion of a liquid or particulate embolic agent in the carotid artery as described by others.17,18 This technique is controversial

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as the residual embolic material may remain in the carotid artery at the time of balloon deflation causing ischemic stroke. A third option is the placement of a covered stent to occlude the ostium of the single arterial feeder to the fistula. Given the young age of the patient and the lack of data on the patency of such stents in the intracranial circulation, it was thought this was not a safe option. The last endovascular option is a transvenous approach via the superior petrosal vein. We thought the open surgical technique was the safest approach with the highest yield of cure for this lesion. A good clinical outcome is dependant on successful obliteration of the leptomeningeal venous drainage, be it from endovascular or surgical means.10,12,19 Surgical therapy has evolved from resection of the nidus to isolated ligation of the venous drainage10,20 with success rates of 87.5% to 100% reported in literature.2,3,8

Conclusion TDAVFs are rare but aggressive and potentially fatal vascular malformations. The clinical presentation depends on the type of venous drainage. The clinical manifestations and neuroimaging findings can mimic other more common neurologic disorders. Early diagnosis is key, as timely intervention can reverse the symptoms and lead to improved clinical outcomes.

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