101.1 Clinical Features
and Laboratory Investigations Cranial dural arteriovenous fistulas (DAVFs) repre- sent 10–15% of all intracranial arteriovenous lesions.
The exact etiology of cranial DAVFs is still unknown.
Development of DAVFs has been described after surgery, head trauma, and in relation to dural sinus thrombosis. In adults, it is generally accepted that DAVFs are acquired conditions. Pediatric cases are rare; DAVFs have infrequently been demonstrated in utero and may be present in neonates, associated with a dural sinus malformation.
Clinical symptoms of DAVFs are related to the fistula itself, e.g., pulsatile tinnitus, or to the venous hypertension in the involved venous territory. The clinical symptomatology and the risk of aggressive complications, such as intracranial hemorrhage, cor- relate directly with the venous drainage pattern of DAVFs. Depending on the venous drainage and the flow characteristics, DAVFs may cause orbital symp- toms including exophthalmia and cranial nerve deficits. A focal area of cortical venous reflux – retro- grade drainage in a cortical leptomeningeal vein – may cause focal neurological deficits, such as aphasia or motor weakness. DAVFs can also cause remote symptoms. Lesions located in the cavernous sinus, tentorium, and foramen magnum can cause venous congestion of the brain stem or spinal cord with relat- ed symptomatology. The retrograde transmission of the arterial pressure in a more extensive venous net- work, in combination with impaired venous outflow through the sinuses, may lead to venous hyperten- sion, resulting in CSF absorption abnormalities and papilledema. These venous pressure disturbances may lead to symptoms of parkinsonism, such as rigidity, bradykinesia, and gait disturbances, and global cognitive dysfunction with dementia as the most severe presentation.
The presence of cortical venous reflux in cranial DAVFs carries an annual mortality rate of 10.4%. The annual risk of hemorrhage is estimated to be 8.1%
per year. The risk of nonhemorrhagic neurological deficit is 6.9% per year. The annual event rate for patients with aggressive DAVFs is therefore 15%.
101.2 Pathology
Histopathologically, DAVFs are located within the wall of the sinus. The fistula itself has no intervening capillary bed or nidus and consists of small venules.
Intimal hyperplasia of both dural arteries and veins is noticed. The arterioles show hypertrophied walls, mainly characterized by media hyperplasia. Orga- nized thrombi have been demonstrated in the dural sinuses in up to 100% of cases.
Immunohistochemically, DAVFs show strong staining for basic fibroblast growth factor (bFGF) in the subendothelial layer and hypertrophied media of the arteries in the sinus wall and in the fibrous connective tissues around the sinuses, sparing the endothelium. Vascular endothelial growth factor (VEGF) stains positively in the endothelium of the dural sinus, small arteries, and veins in the sinus walls. In addition, VEGF stains positively in the en- dothelium of many capillaries in the sinuses that are obstructed by an organized thrombus. No such find- ings are encountered in dural sinuses of control spec- imens. The factors stimulating bFGF and VEGF are not known, but it is postulated that tissue hypoxia and or intraluminal shear stress resulting from ve- nous hypertension stimulates the expression of these angiogenic growth factors.
The acute and chronic parenchymal abnormalities in the case of cortical venous reflux (aggressive type of fistulas) are related to venous hypertension. Acute changes include diffuse cerebral edema and petechial hemorrhages within the gray and white matter.
Chronic changes include markedly dilated and thick- ened, hyalinized walls of the parenchymal veins. Glio- sis may occur within the white matter.
101.3 Pathogenetic Considerations
The association of DAVFs with venous thrombosis has been described frequently. Another important factor contributing to the development of DAVFs is venous or sinus hypertension. Sinus thrombosis does not always lead to the development of DAVFs, and it has been stated that venous hypertension is a pre- requisite for formation of a DAVF, even in the absence of sinus thrombosis. DAVFs have also been reported to develop following intracranial surgery, trauma, surgery in remote areas of the body, and in the post-
Leukoencephalopathy and Dural Arteriovenous Fistulas
R. van den Berg, G.J. Lycklama à Nijeholt, and J.M.C. van Dijk
partum period. The wide variety of etiological factors should not be regarded as direct causes of DAVFs;
rather, they represent environments that may be con- ducive to the development of a DAVF in particular patients.
Two principal theories on the pathogenesis of DAVFs have been proposed. The first claims that DAVFs are caused by enlargement of preexisting mi- crofistulas in the dura. These microfistulas enlarge because of increased venous pressure, associated ei- ther with sinus thrombosis or with sinus outflow ob- struction. The second theory points to the develop- ment of angiogenic factors, such as the above men- tioned bFGF and VEGF, either directly from the orga- nization of a sinus thrombosis or indirectly from local tissue hypoxia due to an increased venous pres- sure.
Many classifications have been proposed for DAVFs, of which the Borden classification and the Cognard classification are most commonly used. The common concept of both classifications is to differen- tiate between DAVFs with antegrade drainage in the dural sinus (benign type: Borden 1, Cognard types I and IIa), and DAVFs with cortical venous reflux (ag- gressive type: Borden 2 and 3, Cognard type IIb and higher) (Table 101.1). The importance of the venous drainage pattern lies in the correlation with clinical symptomatology and the risks of hemorrhage. The retrograde transmission of the arterial pressure in the venous network leads to venous hypertension and congestion and impairs parenchymal venous
drainage. This causes chronic (venous) ischemia. In those cases where extensive reflux is seen in combina- tion with impaired venous outflow through the sinus- es, venous pressures can rise to very high levels.
101.4 Therapy
The natural history of the disease is related to the ve- nous drainage pattern of the DAVF. DAVFs with ante- grade drainage only present with focal symptoms due to the fistula itself, and morbidity and mortality are limited. In these cases treatment should aim only at diminution of the focal symptomatology. DAVFs with cortical venous reflux, however, may lead to severe complications and require aggressive treatment. Dis- connection of the cortical venous reflux is obligatory to protect the patient from sequelae such as intracra- nial hemorrhage and nonhemorrhagic neurological deficits. Partial treatment will not reduce the risk of occurrence of these complications.
Both endovascular embolization and surgery are available to treat DAVFs. Surgical disconnection of the fistulous vein(s) used to be the gold standard for treatment, but with the introduction of liquid adhe- sive embolics, which have been shown to produce a durable result without recanalization, these tech- niques should be regarded as equal. The choice of treatment mode should be decided by the interven- tional neuroradiologist and the neurosurgeon.
If endovascular treatment is chosen, the arterial route is used preferentially. The goal of arterial em- bolization, in which a liquid embolic agent such as n- butyl cyanoacrylate (NBCA) should be regarded as superior to polyvinyl alcohol (PVA) particles, is to penetrate the fistulous point and to occlude the prox- imal part of the refluxing vein. If this cannot be ac- complished, occlusion of the fistulous vein through an alternative route is indicated. The least aggressive is selective disconnection of the refluxing vein(s).
This will leave the DAVF itself untreated. If the fistu- lous zone is more extensive and the cortical venous reflux is found on multiple sites of the dural sinus, or if venous hypertension is the main problem, oblitera- tion of the sinus may be the only treatment option left. However, first a thorough angiographic examina- tion of the venous drainage of the normally draining veins, including the veins of the posterior fossa, is necessary. Sacrifice of the dural sinus can only be per- formed if adequate venous drainage of the brain is guaranteed. Only if the sinus is no longer used for the drainage of the brain parenchyma, and the veins of the posterior fossa do not enter the involved segment, the sinus can be sacrificed.
Selective disconnection of the cortical venous re- flux or sacrifice of (a part of) a dural sinus can also be performed by an open surgical approach or by a com-
Table 101.1. Classification of cranial dural arteriovenous fis- tulas
Borden classification
1. Venous drainage directly into dural venous sinus or meningeal vein
2. Venous drainage into dural venous sinus with cortical venous reflux
3. Venous drainage directly into subarachnoid veins (only cortical venous reflux)
Cognard classification
I. Venous drainage into dural venous sinus with antegrade flow
IIa. Venous drainage into dural venous sinus with retrograde flow
IIa-b. Venous drainage into dural venous sinus with retrograde flow and cortical venous reflux IIb. Venous drainage into dural venous sinus
with antegrade flow and cortical venous reflux III. Venous drainage directly into subarachnoid veins
(only cortical venous reflux)
IV. Type III with venous ectasias of the draining subarachnoid veins
bination of endovascular and surgical approaches. In patients with occlusion of the affected sinus at both proximal and distal sites (isolated sinus), a direct ap- proach to the diseased sinus can be obtained through a small burr hole that allows direct puncture of the dural sinus. Subsequently the fistulous zone of the DAVF can be closed using coils or other thrombo- genic material.
101.5 Magnetic Resonance Imaging
In the presence of a DAVF with cortical venous reflux, unenhanced CT images may show hypodensities, rep- resenting areas of gliosis, edema, or venous ischemia.
Abnormally enlarged pial veins can be depicted due to their increased density compared to the brain parenchyma (Fig. 101.1). Contrast-enhanced CT will show extensive enhancement of the enlarged pial venous network.
In the absence of cortical venous reflux, a DAVF might be occult on MRI. In such cases, the location of the DAVF within the dura and the lack of a mass effect on the brain parenchyma make it very difficult to see the nidus of the fistula on MRI. MRA is more sensitive in depicting the nidus, although the lack of flow infor- mation in time is one of the drawbacks. MRA after injection of a bolus of intravenous contrast may solve this limitation.
In DAVFs with cortical venous reflux MRI shows prominent flow voids on the surface of the brain corresponding to dilated cortical vessels, or more subtle serpiginous or dot-like vascular structures (Fig. 101.2). These are highly suggestive of the correct diagnosis. Hydrocephalus secondary to the venous hypertension in the superior sagittal sinus can be pre- sent. The brain parenchyma, particularly the white matter, may show T2hyperintensity (Fig. 101.2). This is related to venous hypertension and congestion of the brain in the earlier stages and gliosis in later stages. The cerebral involvement may be extensive (Fig. 101.2) or focal (Fig. 101.4). Dependent on the lo- calization of the shunt, the cerebellum, deep gray nu- clei, or brain stem may be affected. DAVFs have been described as the cause of bilateral thalamic hyperin- tensities on T2-weighted images.
The differential diagnosis in bilateral thalamic T2
hyperintensities should include basilar artery infarc- tion, tumor infiltration, and deep venous occlusion.
The differential diagnosis of more diffuse T2hyperin- tensities would include superior sagittal sinus throm- bosis with venous congestion, diffuse glioma, and other leukoencephalopathies. However, the combina- tion of an abundance of dilated pial vessels, contrast enhancement of these vessels, and deep white matter T2 hyperintensity is highly suggestive of a DAVF and mandates further angiographic analysis.
Angiography is obligatory to confirm the diagno- sis DAVF and for treatment planning. Selective con- trast injections into the different branch arteries of the external carotid artery will reveal rapid arteriove- nous shunting through the fistula into the cerebral ve- nous system, thereby arterializing the venous system.
Important concomitant findings are outflow obstruc- tion due to venous sinus occlusion, which can result in extracranial drainage via collateral routes, includ- ing the orbital system, and which augments the risk of retrograde flow into the cortical and cerebellar veins.
The transit time of contrast when injected selectively into the internal carotid artery is delayed, compatible with venous congestion. In the normal situation venous drainage is seen 4–6 s after the beginning of the arterial phase. In addition to the analysis of the venous reflux, the venous drainage of the brain should be examined with the same diligence, not on- ly to detect focal areas of delayed venous drainage, but also to determine whether sacrifice of a dural sinus or a refluxing vein is a potential treatment option.
Fig. 101.1. A 57-year-old man presented with rapid cognitive decline related to a DAVF located in the torcular region. On the plain CT scan dilated pial veins are demonstrated in the right temporal region
Fig. 101.2.
Fig. 101.2. A 67-year-old woman had in her medical history an operation for an acoustic neurinoma on the right. She pre- sented with a rapid cognitive decline.The T2-weighted images (first two rows) show a diffuse signal increase in the deep white matter of both cerebral hemispheres. Abnormal flow voids are visible on the cerebral surface and in the brain parenchyma, especially in the temporal lobes and in the posterior fossa.The T1-weighted images after contrast (third and fourth rows) show extensive enhancement of cortical and parenchymal veins
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Fig. 101.3. Angiography of the pa- tient presented in Fig. 101.2. Selective injection of the external carotid artery (first row, left) shows hypertrophy of the superficial temporal artery and middle meningeal artery. Immediate enhancement of the superior sagittal sinus is seen, suggesting the presence of a DAVF. Selective internal carotid artery injection (first row, right; middle row, left) shows filling of the artery of the falx cerebri through a (hyper- trophied) ophthalmic artery (first row, right). There is early enhancement of the superior sagittal sinus, consistent with a DAVF. There is slow passage of contrast through the brain parenchy- ma because of venous congestion, resulting in a late parenchymal and venous phase. This is also illustrated by the poor visibility of peripheral arteries in the early phase (middle row, left) and by the “pseudo-phlebitic”
aspect of the brain parenchyma in a later phase of the angiogram (middle row, right). After treatment by both an endovascular approach (selective glue injections in external carotid branches feeding the arteriovenous fistula) and by direct placement of coils in the superior sagittal sinus (third row, left;
middle row, right), there is a marked reduction in the size of external carotid artery branches. The internal carotid artery injection after treatment shows abnormal drainage of the brain due to occlusion of the superior sagittal sinus (third row, right). The brain is no longer using the superior sagittal sinus for its drainage. However the transit time of contrast is much shorter. The cognitive symptoms of the patient have dis- appeared almost completely
Fig. 101.4. FLAIR images of a 51-year-old patient who had a single epileptic attack with visual signs.The images show an area of increased signal in the left occipital lobe (second row)
Fig. 101.5. Angiography of the pa- tient presented in Fig. 101.4. Selective injection of the left vertebral artery shows no definite abnormalities (first row), except for nonenhancement of the left transverse and sigmoid sinus. Selective external carotid artery injection shows early filling of a dural tentorial sinus, located in the tentori- um cerebelli, due to a DAVF located there. The fistula is fed by a trans- mastoid branch of the occipital artery (second row, right). There is reflux from the dural sinus into cortical veins in the area (third row), leading to local venous congestion
