Abstract
Dural arteriovenous fistulae (DAVF) constitute 10–15% of all intracranial vascular malformations. As a subtype of DAVF, tentorial DAVF are even rarer, but their aggressive nature warrants early intervention. With regards to symptoms, 70–88% of the cases present with bruits or tinnitus, 60–74% with intracranial haemorrhages, 23–42% with central nerve deficits, 14–17% with cranial nerve deficits, and finally 8–25 % with headaches. Here we report three cases of tentorial DAVF with a primary manifestation of headaches: the first patient is a 44-year-old woman who presented with a severe, persistent sharp occipital headache for 1 day. She deteriorated quickly after admission and required emergency posterior fossa decompression for evacuation of an acute right cerebellar haematoma. Intra-operative and pathological findings suggested a cerebellar arteriovenous malformation. She subsequently underwent transarterial embolisation and surgical excision of the lesion. A review of the histopathological features will be presented. The second case is a 61-year-old male with a 3–4-day history of headache and vomiting prior to presenting to the emergency department with acute delirium secondary to subarachnoid haemorrhage in the posterior fossa. The third case is a 55-year-old woman with moderate, recurrent generalised headaches for 4–5 years. She was managed expediently with transarterial embolisation and had a good outcome. In view of the poor prognosis associated with DAVF rupture, early diagnosis and treatment is warranted to achieve favourable outcomes.
Background
Dural arteriovenous fistulae (DAVF) constitute 10–15 % of all intracranial vascular malformations. 1 DAVF tend to be adult-onset as compared with arteriovenous malformations (AVMs). In adult-type DAVF, there is no true nidus. Instead, DAVF consist of numerous aberrant direct communications between dural arteries and veins without an intervening capillary bed. 2 The precise aetiology of DAVF remains unknown, but is postulated to be an acquired lesion secondary to haemodynamic compromise (e.g. stenosis, thrombosis, and/or occlusion) of the dural venous sinuses. During the recanalisation of the lumen post-insult, microscopic AV shunts that are normally present in the sinus undergo angiogenesis and may enlarge to form numerous microfistulae, which create DAVF. 2 The two commonly used classification systems for DAVF are Borden and Cognard, which correlate angiographic anatomy with clinical presentation outcomes (Table 1).
Classification of DAVF “prognostic values”.
Tentorial DAVF drain through the retrograde leptomeningeal-cortical venous system only (Borden grade III, Cognard grades III and IV), including the cortical or subarachnoid veins, deep drainage through the vein of Galen, and the venous varices. 3 Such drainage patterns result in a high risk of haemorrhage or progressive focal neurological deficits.1,3 Although irradiation, surgical interruption of the vein, transarterial embolisation, and transvenous embolisation are all possible treatment options for DAVF, extensive meningeal arterial supply from the internal carotid artery and vertebral artery, as well as exclusive drainage to the subarachnoid veins, makes the arteries in the region difficult and risky to cannulate and establishing transvenous access a problem.
Case 1
A 44-year-old woman presented with a sudden onset of a severe, persistent sharp occipital headache of 1 day. Her headache was associated with unsteady gait, giddiness, blurring of vision, and vomiting. She denied recent head injury and any loss of consciousness. On general examination, she was lethargic. Cranial nerve examination showed left-beating nystagmus and left-sided dysdiadochokinesis with left-sided past pointing. Pupil diameters were 2 mm bilaterally with brisk pupillary reactions. There were no additional abnormal neurological findings. Computed tomography (CT) imaging was ordered in view of her history of sudden and severe headaches. Upon admission, she rapidly deteriorated to a Glasgow Coma Scale of 7.
Investigations
CT brain
The CT brain showed a hyperdense lesion in the right cerebellar hemisphere with surrounding oedema and mass effect (Figure 1(a, b)). A focal intra parenchymal haematoma was noted in the right cerebellum and the patient underwent emergency posterior fossa decompression, evacuation of the right cerebellar haematoma, and excision of the cerebellar mass. Intra-operatively, the area of interest was noted to be well vascularised. A firm right cerebellar mass was excised and sent for histology. The cerebellum remained pulsatile at the end of the surgery.
(A, B) Initial CT demonstrated a high density “mass” (as illustrated by the arrow), which was originally thought to be a tumour with peri lesional oedema and obstructive hydrocephalus. A repeat CT 4 hours later showed an acute cerebellar haematoma with the “mass” seen within (as illustrated by the arrow), indicating a venous aneurysm. (C) CT angiography after emergency clot evacuation confirmed the presence of the dilated feeding arteries and draining veins of an arteriovenous shunt (as indicated by the arrows). (D) Subsequent catheter angiography showed dilated dural arteries supplying a midline dural AVF with enlarged early filling veins (as emphasised by the asterisk).
Histology
Macroscopically, the specimen was a nodular piece of tissue with a cauterised external surface. The specimen measured approximately 15×11×10 mm. Cut sections revealed a cystic lesion containing blood. The wall was approximately 1 mm in thickness. No thrombus was identified. Histology revealed the lesion to be an apparently ectatic or dilated blood vessel with features of a vein, enclosed within cerebellar tissue. Fibrin coagulum was present within the lumen. Special staining for elastic tissue indicative of arteries or arterialisation was negative. The presence of a discontinuous endothelial lining, at the interface of the wall and its contents, was highlighted by immunostaining for CD34. The smooth muscle cells of the tunica media were confirmed with immunostaining for smooth muscle actin (Figure 2 (a–d)).
Photomicrographs of the lesion excised from the patient reported in Case 1. Staining techniques were as follows: (A) H&E; (B) Elastic van Gieson; (C) CD34 (positive areas indicated by the black arrows); (D) Smooth muscle actin. Scale bar = 2 mm.
Cerebral angiography
A diagnostic angiogram demonstrated a prominent right posterior cerebral artery and cortical venous dilatation at the posterior fossa. Dominant arterial feeders included the bilateral occipital arteries, the distal branch of the right middle meningeal artery, and the right meningohypophyseal arteries. Direct retrograde flow of blood from the fistula into the cortical veins caused venous hypertension, indicating a Borden grade III and Cognard type IV lesion (Figure 1(c)).
Treatment
Transarterial embolisation of the right middle meningeal artery and right occipital artery branch feeders was performed. The former was embolised with 150–255 micron polyvinyl alcohol particles and the latter with Onyx 18 (Figure 1(d)). Immediate post-embolisation images demonstrated satisfactory occlusion of the right occipital artery feeders, with residual feeders coming from the right middle meningeal artery branches and the right meningohypophyseal artery. The flow through the DAVF reduced significantly.
Two months post-procedure, the patient was scheduled for re-admission due to increasing shunting in the persistent right occipital DAVF on a follow-up angiogram. The occipital artery reduced in calibre compared with the previous digital subtraction angiography. The size of the middle meningeal and meningeal branch of the meningohypophyseal arteries remained fairly stable. Interval recruitment of a new feeder from the right occipital artery appeared hypertrophied. Venous drainage had decreased in size compared with the previous diagnostic cerebral angiogram.
On the angiogram, residual-feeding arteries from the right internal carotid artery, right occipital artery, and right middle meningeal artery persisted and continued to drain deeply into the midline vermian veins. Further embolisation was completed in the remnant dural feeders with occlusion of the arterial supply from the right middle meningeal artery using 150–255 micron polyvinyl alcohol particles and the right posterior cerebral artery with Onyx 18. The remaining supply from the meningohypophyseal branch of the right internal carotid artery, a dural branch from left vertebral, and small dural collaterals were noted. Post-embolisation, the patient underwent a posterior fossa craniotomy for complete excision of tentorial DAVF.
Outcome and follow-up
As a result of the occipital haemorrhage, the patient developed right monocular horizontal diplopia with bilateral sixth nerve palsy and moderate oropharyngeal dysphagia. The patient was referred for rehabilitation and continued follow-up with neurosurgery.
Case 2
A 61-year-old man suffered from severe vomiting for 3–4 days and headache prior to acute onset of delirium with incoherent speech and drowsiness. The patient was unable to cooperate for a complete neurological assessment.
Investigations
CT brain
Imaging showed an acute right cerebellar hemisphere and vermian haemorrhage which extended into the fourth ventricle tracking into the third ventricle. Extra-axial haemorrhage was noted in the basal cisterns and along the tentorium cerebelli (Figure 3(a)). Mild left midline shift of the fourth ventricle was present. The lateral and third ventricles were dilated, particularly in the temporal and frontal horns regions, suggestive of hydrocephalus. The patient subsequently had an external ventricular drain inserted.
(A) Coronal CT demonstrated an acute right cerebellar and vermis haemorrhage (as indicated by the arrow). (B) 3D reconstruction from angiography showed feeders from the right vertebral and middle meningeal arteries and dilated inferior vermian vein. (C) The right occipital arteriovenous fistula (as indicated with the asterisk) shown on catheter angiography. (D) Onyx cast (as shown by the arrow) occluded the previously draining arterial feeder at the right occipital artery. Post-embolisation catheter angiography showed no further venous reflux at the dural arteriovenous fistula.
Cerebral angiography
A DAVF was visualised along the midline and was fed by small dural branches from the right vertebral and middle meningeal arteries. Venous drainage primarily went into the inferior vermian vein with venous reflux, indicating a Borden grade III and Cognard type IV lesion (Figure 3(c)).
Treatment
Onyx 18 was used to occlude the middle meningeal artery-feeding vessel up to the proximal segment of the draining vein. A post-embolisation arteriogram showed no residual filling of the DAVF indicating complete occlusion (Figure 3(d)).
Outcome and follow-up
Control angiography at 1-year follow-up showed no residual filling. Complete occlusion of the tentorial DAVF was stable with no recurrences noted. The patient continues to attend outpatient rehabilitation sessions to improve cerebellar ataxia resulting from the initial insult.
Case 3
A 55-year-old woman with a significant history of breast cancer following radiotherapy and traztuzumab treatment suffered from recurrent left-sided generalised headaches associated with left retro-orbital pain for 4–5 years. There was no history of blurring of vision or pulsatile tinnitus. Symptoms persisted despite analgesia. Neurological examination revealed no abnormal findings. In view of her history of breast cancer and the possibility of intracranial metastases, she underwent magnetic resonance (MR) imaging.
Investigations
MR brain
MR imaging demonstrated prominent cortical venous dilatation along the falx cerebelli. There were multiple venous flow voids located at the left side of the cerebellar hemisphere as shown in Figure 4(a, b).
(A, B) The initial T2-weighted MR imaging axial and TiW coronal post-contrast demonstrated dilated cortical veins (as indicated by the arrow) secondary to increased arteriovenous shunting. (C) Catheter angiography of the right occipital artery showed a transcranial feeder leading to the fistula, which was located at the inferior surface of the left tentorium cerebelli. Venous aneurysms and multiple cortical veins over the cerebellar hemisphere were noted. The unsubtracted frame of the angiogram showed the glue cast (as indicated by the asterisk). (D) Subsequent angiography at 1 year confirmed resolution of the venous dilatation and stable occlusion of the DAVF (as indicated by the asterisk).
Cerebral angiography
Angiography revealed a left-sided tentorial DAVF at the junction between the straight and left transverse sinuses. The fistula drained directly into the subarachnoid veins of the left cerebellar hemisphere without passing through the venous sinuses. The fistula was fed by the dominant and largest branches of the left occipital artery, a small branch of the right occipital artery, the neuromeningeal trunk of the right ascending pharyngeal artery, the meningohypophyseal branch of the left internal carotid artery, the V3 segment of the posterior meningeal branch of the left vertebral artery, and a small branch from the petrosquamous branch of the left middle meningeal artery. The dilated venous varix drained towards a single dilated cortical vein into the left transverse sinus. There was stenosis at the confluence of multiple cortical veins into the single dilated vein with retrograde flow, indicative of a Borden grade III and Cognard type IV lesion.
Treatment
Considering the location of drainage, endovascular embolisation was chosen as the preferred modality of treatment over microsurgery. The right occipital artery was embolised with 150–255 micron polyvinyl alcohol particles. The left occipital artery and the petrosquamous branch of the left middle meningeal artery were embolised with Onyx 18 as shown in Figure 4(c). After Onyx embolisation, complete obliteration of the fistula was achieved with cessation of early venous drainage.
Outcome and follow-up
Post-operatively, the patient experienced improvement in her symptoms. However, she continued to have intermittent mild headaches, despite no radiological evidence of recurrence at the 1-year follow-up. Follow-up MR imaging showed a thrombosed venous varix and disappearance of any abnormal flow voids adjacent to the falx cerebelli, as shown in Figure 4(d).
Discussion
Diagnostic dilemma
Due to non-specific clinical symptoms and variable imaging features, tentorial DAVF are difficult to diagnose and often mimic tumours and haematomas in the brain. For our first case, oedema secondary to chronic venous congestion produced an area of low density in the right cerebellum on the non-contrast CT. The subsequent CT showed an acute intracranial haematoma surrounding the hypodense lesion, which led the team to suspect a well-vascularised tumour. Although DAVF are rare, clinicians should keep a high level of suspicion when an intracranial haemorrhage is in an unusual location or presents in an unusual age group.
Biopsy of the partially resected pulsatile tumour from the emergency operation quickly revealed that an AVM might have been the source of haemorrhage. Typical histopathological findings for DAVF specimens were previously described as hypertrophy of dural arteries and veins secondary to proliferation of smooth muscle cells in the tunica media and interna. 4 However, vascular malformations, angiomas, and DAVF are not well classified in pathology. A limited biopsy sample can look like a segment of arterialised veins. Thus, histology alone may not resolve the diagnostic dilemma that tentorial DAVF present. The main limitation from a biopsy is the lack of real-time assessment of the feeder and drainage pattern for the DAVF. Therefore, radiological–pathological correlation is important and necessary for clinicians to arrive at the correct diagnosis.
For our third case, MR imaging was the initial investigation. Diagnosing DAVF on MR imaging is also difficult, particularly for patients with no retrograde venous drainage. Typical DAVF features on MR imaging include dilated cortical veins without a parenchymal nidus, thickened dural leaflets, hypertrophied pachymeningeal arterioles, dilated and tortuous veins, or thrombosed dural sinuses. 5 Arterial supply from multiple small meningeal arteries often cannot be elicited on MR scans. 5
Angiography remains the gold standard for DAVF diagnosis and classification. Other than venous dilatation, enlarged external carotid arteries or transdiploeic vessels may also suggest a diagnosis of DAVF. Systemic evaluation of feeding vessels and demonstration of the extent of retrograde venous drainage is necessary for planning potential interventions.
Tentorial DAVF treatment modalities
Treatment options for tentorial DAVF are based on the Borden and Cognard classification systems (Table 1). Poor natural history is associated with untreated Borden grade II and III DAVF with increased risk of haemorrhage or of non-haemorrhagic neurological deficit. Embolisation usually improves the safety of surgery and may to lead to complete obliteration in some cases. For the most aggressive DAVF, surgery is warranted. Davies et al. confirmed that surgical disconnection alone could cure Borden grade II and III lesions. If cure is not achievable, surgical disconnection can convert an aggressive lesion to a more benign grade I lesion. 6 We have discussed two successful cases of complete DAVF obliteration using polyvinyl alcohol particles and Onyx for arterial and venous embolisations. Endovascular approaches are promising interventions if patients with tentorial DAVF can be identified and treated early on. Here we discuss primary treatments for tentorial DAVF (see Table 2).
Treatment options for tentorial DAVF. 1
Surgery and transarterial embolisation are equal for potential risk and technical difficulty.
Radiotherapy
Unlike other types of DAVF, tentorial DAVF respond poorly to radiotherapy due to their location. The major disadvantage of radiotherapy is the latency of 6–12 months before the DAVF regresses. Furthermore, complete venous occlusion is not always possible. Therefore, radiation therapy is not recommended as the primary therapeutic measure for aggressive tentorial DAVF, despite comparatively lower procedural risk and short-term complications, such as focal neurological deficits and intracranial haemorrhage. 5
Endovascular interventions
Transarterial approach
N-butyl-2-cyanoacrylate depends on its polymerisation rate and viscosity to achieve embolisation. 7 However, n-butyl-2-cyanoacrylate may not reach the DAVF and may instead occlude the proximal feeder. In contrast, polyvinyl alcohol particles are much easier to manipulate. However, recurrence is still relatively high. In a combined approach using polyvinyl alcohol particles and fibre coil, only three out of seven cases (43%) achieved complete occlusion. 8 Thus, polyvinyl alcohol particles are mainly used for palliative reduction of the shunting flow. 7 When adequate arterial routes are available, Onyx is the preferred choice of agents. Onyx’s main disadvantage is the associated mechanical stimulation of the middle meningeal artery in the spinosum foramen, resulting in trigeminal neuralgia. 7 Cognard et al. conducted a prospective study of 30 patients with DAVF and demonstrated complete occlusion using Onyx in 24 cases (80%). 9 Onyx’s ability to form a good cast in both feeders and draining veins make it a primary tool for tentorial DAVF obliteration.9,10
Transvenous approach
Typically highly effective in curing other types of DAVF, the transvenous approach is traditionally avoided in tentorial DAVF due to difficult navigation via tortuous leptomeningeal veins to reach the deep-seated fistula. 7
Surgery
DAVF have extensive arterial supply involving the internal carotid artery and vertebral artery that makes cannulation much more risky and difficult compared with an AVF involving the external carotid artery. 1 When a DAVF drains directly into cortical veins without sinus involvement, surgical disconnection of the arterialised draining veins is possible and results in complete occlusion of the DAVF. Prior to Lawton et al. 3 few published surgical reports described approaches for tentorial DAVF involving the sinuses in depth. Lawton et al. reviewed 31 cases and classified surgical approaches for tentorial fistulae subtypes based on venous drainage routes. 3 Larger cohort studies are needed to validate their findings.
Conclusion
The presentations and outcomes detailed in this report bolster the well-accepted concept that tentorial DAVF are high-risk vascular lesions which warrant immediate intervention. While each treatment modality has its use in specific situations, the option to combine them to achieve better outcomes should always be considered.
Footnotes
Declaration of Conflicting Interest
None declared.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.