Case record...Multiple dural arteriovenous fistulas http://yassermetwally.com http://yassermetwally.net

1. CASE OF THE WEEK
PROFESSOR YASSER METWALLY
CLINICAL PICTURE
CLINICAL PICTURE:
A 29 years old male patients presented with proptosis , ecchymoses of the
left eye with both subjective and objective bruit in the left eye and and left
ear, and tinnitus in the left ear. Ther was no history of trauma, venous
thrombosis, of surgical operations. The condition is dated since birth.
RADIOLOGICAL FINDINGS
RADIOLOGICAL FINDINGS:
Figure 1. Postcontrast CT scan showing a left temporal dilated venous channels with some wall calcifications and
moderate mass effect. The densely enhanced venous channels are mixed with parenchymal hypodensities. The dilated,
densely enhanced venous channel reflects venous hypertension which commonly results in retrograde venous reflux,
congestive encephalopathy and white matter changes (petechial hemorrhages, white matter edema, reactive
astrogliosis). Dilated venous pouches with all calcification are evident in (A)

2. Figure 2. Postcontrast CT scan showing a left hemispherical markedly dilated, densely enhanced venous channels
(venous ectasia). The disease is involving both then superficial (Cortical) and deep venous systems. Both systems are
interconnected by transhemisperical dilated collaterals. The dilatation predominately affects the deep venous system.
The white matter changes most probably reflects retrograde venous reflux and congestive encephalopathy. The dilated
transhemisperical venous channels and congestive encephalopathy most probably denotes the existence of cortical
venous reflux. Notice the marked dilations of the the vein of Galen.
Figure 3. Precontrast MRI T1 images showing markedly dilated signal void tortuous venous channels predominately
involving the deep venous systems of the left hemisphere, with some dilated cortical veins, in particular the vein of
Galen is markedly dilated. Notice the significant white matter changes in the form of a mixture of T1 hypointensities,
hyperintensities and positive mass effect. The precontrast T1 hyperintensities most probably represents blood
products secondary to venous congestion.

3. Figure 4. MRI T2 images showing markedly dilated signal void tortuous venous channels predominately involving the
deep venous systems of the left hemisphere, with some dilated cortical veins, in particular the vein of Galen is
markedly dilated. Notice the significant white matter changes in the form of a mixture of T2 hypointensities,
hyperintensities and positive mass effect. The term venous congestive encephalopathy (VCE) was introduced in 1994.
On CT, the venous congestion may be evident as an area of edema and mass effect. In patients with cortical venous
reflux , MR imaging often shows prominent flow voids on the surface of the brain. Hydrocephalus may be secondary
to the venous hypertension in the superior saggital sinus. On MR imaging, T2 hyperintensity deep in the brain
parenchyma may be evident secondary to the venous hypertension and passive congestion of the brain. The
cerebellum, cerebrum, and deep gray nuclei or brainstem may be affected. In chronic cases, the proton density or T2-
weighted images may show a central hypointensity that may be related to hemosiderin deposition from chronic venous
congestion. In the cerebral hemispheres, the deep white matter is the most vulnerable to the venous congestion. The T2
hyperintensity may be reversible after treatment. The differential diagnosis of the T2 hyperintensity would include a
superior sagittal sinus thrombosis with a venous infarction or venous congestion, demyelination, or a dysmyelination
and neoplasm. But the combination of a surplus of pial vessels, T2 hyperintensity deep within the brain, and
peripheral enhancement is highly suggestive of a dural arteriovenous fistula and mandates prompt angiography.
Figure 5. MRI T2 images showing markedly dilated signal void tortuous venous channels predominately involving the
deep venous systems of the left hemisphere, with some dilated cortical veins, in particular the vein of Galen is
markedly dilated. Notice the significant white matter changes in the form of a mixture of T2 hypointensities,

4. hyperintensities and positive mass effect. The term venous congestive encephalopathy (VCE) was introduced in 1994.
On CT, the venous congestion may be evident as an area of edema and mass effect. In patients with cortical venous
reflux , MR imaging often shows prominent flow voids on the surface of the brain. Hydrocephalus may be secondary
to the venous hypertension in the superior saggital sinus. On MR imaging, T2 hyperintensity deep in the brain
parenchyma may be evident secondary to the venous hypertension and passive congestion of the brain. The
cerebellum, cerebrum, and deep gray nuclei or brainstem may be affected. In chronic cases, the proton density or T2-
weighted images may show a central hypointensity that may be related to hemosiderin deposition from chronic venous
congestion. In the cerebral hemispheres, the deep white matter is the most vulnerable to the venous congestion. The T2
hyperintensity may be reversible after treatment. The differential diagnosis of the T2 hyperintensity would include a
superior sagittal sinus thrombosis with a venous infarction or venous congestion, demyelination, or a dysmyelination
and neoplasm. But the combination of a surplus of pial vessels, T2 hyperintensity deep within the brain, and
peripheral enhancement is highly suggestive of a dural arteriovenous fistula and mandates prompt angiography.
Figure 6. MRI T2 images showing markedly dilated signal void tortuous venous channels predominately involving the
deep venous systems of the left hemisphere, with some dilated cortical veins, in particular the vein of Galen is
markedly dilated. Notice the significant white matter changes in the form of a mixture of T2 hypointensities,
hyperintensities and positive mass effect. The term venous congestive encephalopathy (VCE) was introduced in 1994.
On CT, the venous congestion may be evident as an area of edema and mass effect. In patients with cortical venous
reflux , MR imaging often shows prominent flow voids on the surface of the brain. Hydrocephalus may be secondary
to the venous hypertension in the superior saggital sinus. On MR imaging, T2 hyperintensity deep in the brain
parenchyma may be evident secondary to the venous hypertension and passive congestion of the brain. The
cerebellum, cerebrum, and deep gray nuclei or brainstem may be affected. In chronic cases, the proton density or T2-
weighted images may show a central hypointensity that may be related to hemosiderin deposition from chronic venous
congestion. In the cerebral hemispheres, the deep white matter is the most vulnerable to the venous congestion. The T2
hyperintensity may be reversible after treatment. The differential diagnosis of the T2 hyperintensity would include a
superior sagittal sinus thrombosis with a venous infarction or venous congestion, demyelination, or a dysmyelination
and neoplasm. But the combination of a surplus of pial vessels, T2 hyperintensity deep within the brain, and
peripheral enhancement is highly suggestive of a dural arteriovenous fistula and mandates prompt angiography.

5. Figure 7. MRA study showing markedly dilated deep venous systems with prominent transhemisperical venous
channels probably reflecting cortical venous reflux. The superior sagittal sinus is also probably dilated.
Figure 8. MRA study showing markedly dilated deep
venous systems with prominent transhemisperical
venous channels probably reflecting cortical venous
reflux.
The primary pathology in the above reported case is two dural arteriovenous fistulas at the cavernous sinus and the

6. segmoidal sinus resulting in venous hypertension, dilatations, tortuosity and remodeling of the deep venous system,
with cortical venous reflux and congestive encephalopathy.
Abnormal communications between the arterial and venous systems may be congenital or acquired. Most extracranial
arteriovenous malformations (AVMs) are apparent clinically, although imaging studies are helpful in delineating the
extent of the abnormality. Brain parenchymal arteriovenous malformations may be more obscure clinically, but are
usually quite readily identified on contrast-enhanced CT and MR studies. Conventional angiography identifies arterial
supply and venous drainage. CT angiography may also prove useful. Time-of-flight MR angiography complements
spin-echo sequences.
A dural AVM or arteriovenous fistula (AVF) is a well-known cause of headache and hemorrhagic infarction. However,
dural AVM or arteriovenous fistula is also the most frequent cause of objective pulsatile tinnitus in the patient with a
normal otoscopic examination. The transverse, sigmoid, and cavernous sinuses are the most frequent locations of dural
arteriovenous malformations and arteriovenous fistulas; transverse and sigmoid sinus involvement causes pulsatile
tinnitus. Branches of the external carotid artery supply these dural arteriovenous malformations; venous drainage
may be extracranial, intracranial, or both.
CT or MR studies may demonstrate a dilated dural venous sinus, unusually large or numerous cortical veins, or
abnormal vessels in the soft tissues beneath the skull base. However, dural arteriovenous malformations or
arteriovenous fistulas are often invisible on CT and MR studies. A normal contrast-enhanced CT or MR study
therefore does not exclude a dural AVM or AVF. Conventional angiography may be the only modality that shows the
abnormality. When a patient has convincing history and physical findings and normal cross-sectional imaging studies,
conventional angiography is an important diagnostic option.
Brain arteriovenous shunts (AVSS) develop from a primary defect or malformation of the neurovascular system.
There are two broad categories of Brain arteriovenous shunts: arteriovenous malformations (AVMS) and
arteriovenous fistulas (AVFs). Brain arteriovenous shunts are characterized by the direct connection of one or more
arteries to one or more draining veins, without intervening capillary beds. The shunting of arterial blood into the low-
resistance venous network produces a high flow that typifies these lesions and results in distention, tortuosity, and
reactive changes in the affected arteries and veins.
The venous compartment of brain arteriovenous shunts is relatively difficult to evaluate, even on angiography,
compared with the arterial or nidal compartments, because of superimposed venous outlets and poor opacification of
the draining veins. Venous stenosis, venous dilatation, deep venous drainage, and venous reflux have been reported to
be potential risk factors for hemorrhagic events. Analysis of the venous compartment is crucial for the evaluation and
management of patients with the brain arteriovenous shunts.
The radiologic findings of the venous compartment of brain arteriovenous shunts include developmental variations,
suggesting a congenital origin of the disease, and secondary responses to the brain arteriovenous shunts, such as
collaterals. These structural changes can be regarded as the anatomic adaptations to high-flow shunts. Thus, the
radiologic findings are extremely variable according to the hemodynamics and are modified by the development of
venous stenosis or ectasia.
The venous ectasia of brain arteriovenous shunts is a progressive response of the venous wall to the high-flow
situation. Thus, this anatomic change is regarded as a failure to find an efficient exit to relieve the increased pressure.
The venous ectasia can be defined as quot;any change in venous caliber in the venous runoff or drainage from the brain
arteriovenous shunts, with a >2-fold caliber change in any draining venous channelquot;. The venous stenosis is defined as
a narrowing of any draining venous outflow pathway in two angiographic views. Focal venous ectasia (venous pouch)
can resemble a cystic intracranial mass lesion. Because there is little evidence that most brain arteriovenous shunts are
present at birth, cystic intracranial lesions during the intrauterine or neonatal period seen by ultrasonography can
easily be misinterpreted as arachnoid cysts or cystic brain neoplasms. Further investigations, such as with Doppler
unltrasonsography or MRI, might be considered to differentiate the previously described diagnostic possibilities.
Venous pouches are one of characteristic findings in patients with hereditary hemorrhagic telangiectasia (HHT) who
have brain arteriovenous fistulas. A large venous pouch on MRI and multiple brain arteriovenous shunts should raise
the suspicion of HHT. In the author experience, multiple brain arteriovenous malformations in the same patient
occurred in 50% of the patients with HHT.
Venous ectasias can becomes so large that they cause local or generalized mass effect and symptoms of increased
intracranial pressure. Large venous pouches are more frequently seen in children with brain arteriovenous shunts
compared with adults. In adults, large venous ectasias may reflect the size of the malformation and the insufficient

7. number of draining veins from such large shunts.
Anatomic venous obstacles, such as the tentorial ridge, deep sylvian fissure, or Monro foramen, may compress the
draining vein directly. This results in a proximal stenosis with distal ectasia of the draining vein. When the
compression is caused by bridging arteries, however, the venous stenosis may not be associated with an upstream
ectasia. In addition, converging venous systems (deep venous systems, posterior portion of the basal vein, and deep
Sylvian vein) have a higher chance of developing venous ectasias than do diverging venous systems, such as cortical
veins.
Thrombosis of the venous drainage pathway also represents a venous flow disturbance. The draining vein may
thrombose partially or completely. The sequential CT and MRI examinations may show progressive clot formation
within the venous compartment of an brain arteriovenous shunts. With partial or complete thrombosis of a common
venous channel for both the surrounding brain parenchyma and brain arteriovenous shunts, brain edema may be
demonstrated.
Angiography seldom reveals a partially thrombosed vein but may show a relatively delayed visualization of the venous
compartment of the brain arteriovenous shunts. If the brain arteriovenous shunts has more than one draining vein and
some of them are thrombosed, the shunted blood flow may be rerouted to a nonthrombosed draining vein or veins or
recruit adjacent veins that have not been used by the brain arteriovenous shunts. Because the drainage of brain
arteriovenous malformations is usually predictable from the location of the nidus, unusual venous drainage patterns
for the nidus location may suggest partial or complete thrombosis of the venous compartment of the brain AVM.
The venous reflux into a sinus or a deep vein has been reported to be a risk factor for hemorrhagic events. Venous
reflux into the cortical veins can also be demonstrated on angiography. The venous reflux should be differentiated
from venous collaterals. The venous reflux is the reversal of flow in any venous outflow pathway in a direction other
than the normal pathway, but venous collaterals maintain their normal drainage pathway.
DIAGNOSIS:
DIAGNOSIS: MULTIPLE DURAL ARTERIOVENOUS FISTULAS IN THE TRANSVERSE SEGMOIDAL SINUS
AND CAVERNOUS SINUS.
DISCUSSION
DISCUSSION:
Cranial dural arteriovenous fistulas (DAVFs) are a unique neurovascular entity, representing 10-15% of all
intracranial arteriovenous lesions [1]. In the literature many dural arteriovenous fistulas have been referred to as
quot;malformationsquot; in adults, however, we prefer the term quot;fistulasquot;. dural arteriovenous fistulas consist of one or more
direct arteriovenous connections within the dura mater. This anatomic location clearly discerns dural arteriovenous
fistulas from the pial arteriovenous malformations (AVMs). It is generally accepted that dural arteriovenous fistulas
are acquired [2-5] as opposed to the pial arteriovenous malformations that are thought to be congenital [6,7]. The rare
exception is in the pediatric age group where congenital dural malformations are associated with high-flow single or
multifocal fistula.
DAVFs can be found anywhere along the dura mater, both cranial and spinal. Spinal dural arteriovenous fistulas
present with a chronic progressive myelopathy caused by venous hypertension in the perimedullary venous plexus.
There are only a few reports of hemorrhage related to a spinal dural arteriovenous fistula, and these rare lesions are in
the craniocervical location [8]. By contrast, cranial dural arteriovenous fistulas present with a diverse spectrum of
clinical signs and symptoms including hemorrhage. The clinical findings in intracranial dural arteriovenous fistulas
may be related to the fistula itself (ie, bruit) or the venous hypertension in the involved venous territory. The venous
hypertension can involve the orbit or the brain depending on the venous drainage. If the brain is involved, both
hemorrhagic and nonhemorrhagic neurologic deficit can occur.
History

Dural arteriovenous fistulas were rarely identified before 1960. In the seventies, dural arteriovenous fistulas were
recognized as a distinct entity caused by the advances in angiography that included magnification, subtraction
techniques, and selective arterial catheterization [9]. At first, these dural lesions were regarded as a benign disease in

8. comparison with pial arteriovenous malformations [10,11]. Aminoff [12], Newton [1], and Djindjian [13] deepened the
anatomic and clinical knowledge regarding dural arteriovenous fistulas. In 1972, it was recognized that the pattern of
venous drainage could be related to the clinical signs and symptoms [9]. In 1975, Castaigne et al highlighted the risks
of cortical venous drainage (CVR) [14]. Djindjian et al proposed the first classification of dural arteriovenous fistulas
based on the venous drainage, stating that dural arteriovenous fistulas with a free outflow into a sinus were relatively
harmless, whereas lesions with cortical venous reflux could produce severe complications [15].
In 1984, Malik et al [16] published their review of 223 cases, emphasizing that restriction of venous outflow was a key
factor in the clinical expression of the disease. They did not emphasize, however, the importance of the cortical venous
reflux. Lasjaunias et al [17] published a meta-analysis of 191 cases in addition to their four illustrative cases,
concluding that focal neurologic symptoms were dependent on the territory of the draining veins, and that cortical
venous reflux carries a high risk of intradural bleeding. Awad et al [18] reviewed 377 cases, mostly from the literature,
and introduced the term quot;aggressivequot; for lesions presenting with a hemorrhage or a focal neurologic deficit. Awad et
al also emphasized the importance of cortical venous reflux and included venous ectasias and galenic drainage as risk
factors for an aggressive course.
Pathogenesis

The etiology of cranial dural arteriovenous fistulas is unknown. Dural arteriovenous fistulas have been described after
surgery, head trauma, and in relation to sinus thrombosis. Two hypotheses of the pathogenesis have been proposed.
The first hypothesis claims that cranial dural arteriovenous fistulas arise from already existing quot;dormantquot; channels
between the external carotid circulation and the venous pathways within the dura mater. Histopathologic and
radioanatomic studies have shown that these communications are normally present in the dura [19]. These channels
open because of the venous hypertension associated with sinus thrombosis or sinus outflow obstruction [4,12,15,18,20].
A variation to this theme is the reported existence of thin-walled venous pouches within the dura, close to small
arteries. Rupture of these fragile pouches easily induces arteriovenous communications within the dura [21,22]. The
second hypothesis claims that dural arteriovenous fistulas are the result of new vascular channels that are stimulated
by angiogenetic factors. These factors, such as VEGF and bFGF, originate either directly from the organization of a
sinus thrombosis or indirectly because of tissue hypoxia related to an increased intraluminal venous pressure [3,5,23-
25].
Histopathologically, the true arteriovenous fistula has no intervening capillary bed and consists of small venules with a
diameter of approximately 30μ. These vessels have been called quot;crack-like vessels,quot; because they look like cracks in
the dural sinus wall after histologic staining [26]. Furthermore, intimal thickening of both dural arteries and dural
veins has been observed [27]. Although the fistula initially has been described within a thrombosed sinus, it is generally
accepted that the fistula is located within the wall of the sinus. This explains the existence of dural arteriovenous
fistulas that drain directly into the pial venous network [25,28].
Classification

The terms quot;benignquot; and quot;aggressivequot; can be applied to the symptomatology and natural history of cranial dural
arteriovenous fistulas [18,29-32]. Nonhemorrhagic neurologic deficits (NHND), hemorrhage, and death are considered
aggressive. Chronic headache, pulsatile bruit, and orbital symptoms including cranial nerve deficit are considered
benign.
The anatomic location of a dural arteriovenous fistula initially was felt to be important in its association with the
venous drainage pattern and symptomatolgy [33]. Cavernous sinus and transverse sinus lesions often have sinosal
drainage only, whereas anterior cranial fossa and tentorial lesions almost all have cortical venous reflux. Recently, it
has become evident that any location can develop cortical venous reflux , including the cavernous sinus and transverse
sinus locations. Aminoff grouped dural arteriovenous fistulas by location, separating them into an anteroinferior
group and a posterosuperior group [12]. Later, authors pointed out a relationship between the location of the dural
arteriovenous fistula and the behavior of the dural arteriovenous fistula [18,34]. Malik et al hypothesized that dural
arteriovenous fistulas in specific locations have a higher likelihood of developing cortical venous reflux [16]. Malik et al
related cortical venous reflux to the presence or absence of a dural sinus at the site of the fistula. Although no location
is immune from aggressive behavior [18], certain locations are more prone to have cortical venous reflux.
Several classification schemes for cranial dural arteriovenous fistulas have been introduced [15,35-37]. Classification
schemes must be used with caution because dural arteriovenous fistulas are a dynamic process and their
angioarchitecture can be altered by venous thrombosis. The classifications of Borden et al and Cognard et al are the
most widely used (Table 1). Although the three-step classification of Borden has the advantage of being relatively

9. simple to apply, the Cognard classification (a revision of the Djindjian classification scheme) incorporates the
additional influence of retrograde flow in the sinus and spinal venous drainage. Retrograde flow can prohibit the
cortical veins from draining into the involved sinus because of venous hypertension in the sinus leading to venous
congestion of the brain without cortical venous reflux. Both classifications have been validated by Davies et al [33].
Borden 1, Cognard I, and Cognard IIa lesions are considered benign, whereas all other Borden and Cognard grades
should be considered aggressive.
Table 1. Classification of cranial dural arteriovenous fistulas
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 (cortical venous reflux only)
Cognard classification
I Venous drainage into dural venous sinus with antegrade flow
IIa Venous drainage into dural venous sinus with retrograde flow
IIb Venous drainage into dural venous sinus with antegrade flow and cortical venous reflux
IIa + b Venous drainage into dural venous sinus with retrograde flow and cortical venous reflux
III Venous drainage directly into subarachnoid veins (cortical venous reflux only)
IV Type III with venous ectasias of the draining subarachnoid veins
Abbreviation: CVR; cortical venous reflux.
In the pediatric age group, Lasjaunias has recognized three types of dural arteriovenous fistulas [6]. These include the
dural sinus malformations with arteriovenous shunting, infantile dural arteriovenous shunts, and the adult-type dural
arteriovenous fistulas. The dural sinus malformations and high-flow infantile arteriovenous shunts in the pediatric age
group are beyond the scope of this article.
Symptomatolgy

The majority of the fistulas present with the so-called quot;benignquot; symptoms, either a pulsatile tinnitus or orbital
congestion (Table 2). The patients with pulsatile tinnitus usually have an objective bruit (Fig. 9). Other than pulsatile
tinnitus, the symptoms relate to the venous drainage of the fistula and are commonly remote from the fistula itself.
Fistulas can present at any age, although patients are often over 50 years of age. Adult-type dural arteriovenous
fistulas in childhood are rare. Patients presenting with orbital congestion frequently have cavernous sinus dural
arteriovenous fistulas (Fig. 10). The orbital signs include chemosis, conjunctival injection, and proptosis. The orbital
symptoms may be progressive and to the patient may not be considered quot;benign.quot; Patients may develop an
ophthalmoplegia related to a cranial nerve dysfunction or extraocular muscle swelling. Orbital congestion may result
in raised intraocular pressure and lead to loss of visual acuity.
Table 2. Clinical findings in cranial dural arteriovenous fistula
Common signs and symptoms
Pulsatile tinnitus
Objective bruit
Proptosis, conjunctival injection, chemosis
Ophthalomoplegia
Visual loss
Glaucoma
Transient ischemic attacks
Aphasia
Motor weakness

10. Dementia
Papilledema
Intracranial hemorrhage
Figure 9. quot;Benignquot; type dural
arteriovenous fistula in a 40-year-old
male patient with pulsatile tinnitus.
(A) Lateral left ascending pharyngeal
artery (straight arrow) and (B) left
occipital artery (straight arrow)
angiograms show a network of arterial
branches participating in a shunt into
the jugular bulb (curved arrow) (A)
and sigmoid sinus (curved arrow) (B).
Figure 10. Anterior cavernous sinus dural arteriovenous fistula. Transvenous endovascular treatment in 36-year-old
female patient with visual loss. (A) Coronal T1-weighted and (B) T2-weighted MR image show an enlarged superior
ophthalmic vein (arrow) (A) and a dilated inferior lateral trunk artery (ILT) (arrow) (B). (C) Lateral internal carotid

11. artery angiogram shows a high-flow shunt into the anterior cavernous sinus (open arrow) and drainage exclusively into
the orbit. (D) Lateral radiograph shows a microcatheter (small arrows) coursing through the transverse facial vein and
superior ophthalmic vein. Coils (solid arrow) have been deposited into the cavernous sinus at the fistula site. (E)
Postembolization lateral internal carotid angiogram shows that the fistula is closed.quot;Aggressivequot; symptoms include
neurologic dysfunction related to intracranial hemorrhage or venous congestion. The hemorrhage can be
subarachnoid, subdural, or intracranial. The neurologic dysfunction can include aphasia, weakness, transient ischemic
attacks, seizures, and dementia. Papilledema and communicating hydrocephalus can be presenting findings. Heart
failure and craniomegaly are only seen in the dural sinus malformations and infantile dural arteriovenous fistulas of
childhood.
Location

The location of dural arteriovenous fistula is defined by the site of the arteriovenous shunting. The venous drainage of
the fistula is influenced by the degree of venous obstruction of the involved venous sinus. Direct fistulas into cortical
veins result from complete obstruction of the adjacent sinus. Table 3 outlines the common locations of dural
arteriovenous fistulas and their venous drainage. The venous drainage is variable and may evolve with time. Change in
the venous drainage is caused by venous thrombosis or may be the consequence of a hemorrhage.
Table 3. Common locations of cranial dural arteriovenous fistula and their venous drainage
Location Venous drainage
Anterior cranial
Frontal and olfactory veins
fossa
Anterior cavernous
Ophthalmic and deep sylvian veins
sinus
Posterior cavernous Superior and inferior petrosal sinuses; ophthalmic, deep sylvian, uncal and anterior
sinus pontomesencephalic veins
Sphenoid wing Deep sylvian veins
Transverse sinus Sigmoid sinus; temporal and cerebellar veins
Torcula Transverse sinus; medial occipital and infratemporal veins
Tentorial Basal vein of Rosenthal, lateral mesencephalic and tentorial veins
SSS SSS; cortical veins
Inferior straight
Vermian veins
sinus
Foramen magnum Marginal sinus; lateral pontomesencephalic and spinal veins
Abbreviation: SSS; superior saggital sinus.
TYPES OF CRANIAL DURAL ARTERIOVENOUS FISTULAS
Benign fistulas

Awareness of the natural history of a given disease is essential for patient management. The results of any active
treatment must be compared with the outcome of the natural history of that disease. The recognition of the so-called
benign fistulas is helpful in planning a management strategy; the evolution of the disease must be carefully monitored,
however. A change in symptomatology may be related to either reduced flow through the malformation or rerouting of
the venous drainage. A fistula that originally had anterograde sinosal drainage could convert to a fistula with
retrograde sinosal drainage or develop cortical venous reflux.
In the absence of cortical venous reflux , cranial dural arteriovenous fistulas have a benign presentation and, in most
cases, an uneventful clinical course [33,38]. There are only three publications focused on the natural history and
angiographic follow-up of dural arteriovenous fistulas without cortical venous reflux. Davies et al [29] reported their
experience with a cohort of 54 cases without cortical venous reflux over a mean follow-up period of 33 months. Only
one of the cases (2%) died after palliative endovascular treatment; there was, however, no evidence of angiographic
conversion into a lesion with cortical venous reflux. This unusual course resulted from the development of venous
hypertension caused by functional obstruction of the superior sagittal sinus. In conclusion, Davies et al reported that

12. the majority of cranial dural arteriovenous fistulas without cortical venous reflux behave in a benign fashion and that
the focus of therapeutic efforts, if necessary, should be directed toward palliation rather than toward angiographic
cure. Over 80% of the patients not treated had clinical improvement during the mean follow-up of over 2 years.
Cognard et al [39] reported seven patients that initially had a dural arteriovenous fistula without cortical venous
reflux and later converted to a dural arteriovenous fistula with cortical venous reflux. The rate of conversion of dural
arteriovenous fistulas without cortical venous reflux to those that develop cortical venous reflux cannot be ascertained
as the total number of patients was not included in the report. Five patients were embolized with particles, one patient
had proximal ligation of the occipital and middle meningeal artery, and one patient had conservative management. All
of them showed a worsening in the venous drainage pattern during a follow-up between 1 month and 20 years (mean, 7
years). Two cases, both embolized, demonstrated a change from antegrade to retrograde flow into the draining sinus,
and five cases developed cortical venous reflux. In all cases, the change in venous pattern was accompanied by a
worsening of the clinical symptoms.
In a more recent study by Satomi et al [31], the chronologic change in clinical symptoms and angiographic features of
117 patients harboring cranial dural arteriovenous fistula without cortical venous reflux were evaluated. None of the
cases presented with either intracranial hemorrhage or Nonhemorrhagic neurologic deficits, and the majority of these
lesions were managed conservatively. Palliative treatment, never aimed at cure, was performed if the patient had
intolerable symptoms or if there was a persistent high intraocular pressure or decreasing visual acuity. Sixty-three
percent of the patients had no invasive treatment. Using this conservative management, 98% of the patients had a well-
tolerated clinical course. In Satomi et al's series, five cases showed a change in their venous drainage pattern
associated with progressive thrombosis of the venous outlets during the follow-up period. Three patients with
cavernous sinus dural arteriovenous fistulas (conservative management in 1 case, palliative embolization in 2 cases)
had an alteration in sinus drainage direction from antegrade to retrograde, after which the lesions eventually resolved
spontaneously. The two other cases showed angiographic conversion into a lesion with cortical venous reflux , with
symptom resolution in one case and symptom aggravation in the other. This demonstrates that dural arteriovenous
fistulas without cortical venous reflux have the potential to develop cortical venous reflux even without treatment. All
five cases with angiographic conversion were associated with progressive steno-occlusive change in the affected sinus
without arterial flow increase or de novo arteriovenous shunts. Stenosis or thrombosis of the secondarily occluded
venous outlets was not present on the initial angiogram in these cases.
In conclusion, the disease course of a cranial dural arteriovenous fistula without cortical venous reflux is benign in
most cases, obviating the need for a cure of these lesions. Symptoms are well tolerated with either observation or
palliative treatment. A dural arteriovenous fistula of the benign type has a 2-3% potential of developing cortical
venous reflux , however, mandating close clinical follow-up and renewed radiologic evaluation with any deterioration
or change in symptoms.
Aggressive fistulas

Cranial dural arteriovenous fistulas with cortical venous reflux are considered aggressive lesions. They often present
with intracranial hemorrhage or Nonhemorrhagic neurologic deficits [4,14,16-18]. The disease course after their
aggressive presentation is less well understood, however. The only studies predominantly focused on events after
presentation were performed by Duffau et al [40], Brown et al [34], and Davies et al [30]. Duffau et al looked at their
short time frame between the diagnosis and treatment, which lasted a mean of only 20 days. Brown et al followed
patients for mean 6.6 years but did not specifically select for cortical venous reflux. In 1997 Davies et al [30] calculated
an annual mortality of 19.2%, with a 19.2% annual rate of hemorrhage and a 10.9% annual rate of Nonhemorrhagic
neurologic deficits during the disease course of dural arteriovenous fistulas with persistent cortical venous reflux. A
recalculation of Davies et al's series was performed in 2002 by Van Dijk et al [32], based on a larger population and
four times the follow-up time. This yielded an annual mortality rate of 10.4%. In addition, disregarding aggressive
events at presentation, the annual risk of intracranial hemorrhage or Nonhemorrhagic neurologic deficits was 8.1%
and 6.9%, respectively, adding up to a 15.0% annual adverse event rate. These numbers mandate a prompt, accurate
diagnosis and treatment of these aggressive lesions.
NEUROIMAGING OF CRANIAL DURAL ARTERIOVENOUS FISTULAS
Dural arteriovenous fistulas without cortical venous reflux

MR imaging of the brain parenchyma in patients with dural arteriovenous fistulas without cortical venous reflux is
typically normal. The involved dural sinuses may be irregular, stenotic, or septated on MR imaging. MR angiography
may confirm the occlusive changes within the involved sinus. Hydrocephalus may be present in any dural

13. arteriovenous fistula that causes venous hypertension in the superior sagittal sinus. The venous hypertension may
result from retrograde flow in the superior sagittal sinus. Cortical venous reflux may not be present. The venous
hypertension interferes with the cerebrospinal fluid absorption by the pacchionian granulations.
Dural arteriovenous fistulas with cortical venous reflux

MR imaging is often positive in dural arteriovenous fistulas with cortical venous reflux. In Willinsky et al's review, 10
of the 13 patients (77%) with dural arteriovenous fistulas and cortical venous reflux had dilated pial vessels. Two
patients had hydrocephalus. Diffuse white matter edema, in the cerebellar or cerebral hemispheres, was present on
MR imaging in 4 patients and correlated with neurologic deficits. In two of these four patients gadolinium
enhancement surrounding the area of T2 hyperintensity was seen in the periphery of the involved hemisphere.
Figure 11. Cerebellar venous congestion secondary to a straight sinus dural arteriovenous fistula with cortical venous
reflux. (A) T2-weighted MR image shows central hyperintensity (open arrow) in the cerebellar hemisphere with
peripheral hypointensity and prominent flow-voids (closed arrows). (B) T1-weighted gadolinium-enhanced MR image
shows peripheral enhancement adjacent to the T2 hyperintense lesion. (C) Early and (D) late phases of the selective
angiogram of a dural branch (small arrows) of the right vertebral artery show a fistula in the wall of the straight sinus.
The drainage is retrograde into the inferior vermian vein (large arrows) that then refluxes into the cerebellar
hemisphere veins (D).

14. Figure 12. Post-treatment resolution of venous congestion. (A) FLAIR MR image shows central hyperintensity (arrow)
in the cerebellum. (B) Gadolinium-enhanced MR image shows peripheral enhancement (arrow) surrounding the
hyperintense region seen on the FLAIR. (C) Lateral right vertebral angiogram shows a dural arteriovenous fistula
(open arrow) fed by a dural branch (arrowhead) of the vertebral artery and draining into the inferior vermian vein
(curved arrow). (D) Late phase of the AP right vertebral angiogram shows a PPP in the right cerebellar hemisphere
related to venous congestion. (E) Posttreatment (embolization and surgery) FLAIR MR image shows resolution of the
venous congestion.
The term venous congestive encephalopathy (VCE) was introduced in 1994 to describe those patients who present with
cranial neurologic deficits caused by venous hypertension [41]. This entity is analogous to the venous congestive
myelopathy of the spinal cord in the presence of a spinal dural arteriovenous fistula [42]. On CT, the venous
congestion may be evident as an area of edema and mass effect. In patients with cortical venous reflux , MR imaging
often shows prominent flow voids on the surface of the brain). Hydrocephalus may be secondary to the venous
hypertension in the superior saggital sinus. On MR imaging, T2 hyperintensity deep in the brain parenchyma may be
evident secondary to the venous hypertension and passive congestion of the brain. The cerebellum, cerebrum, and
deep gray nuclei or brainstem may be affected. In chronic cases, the proton density or T2-weighted images may show a
central hypointensity that may be related to hemosiderin deposition from chronic venous congestion. In the cerebral
hemispheres, the deep white matter is the most vulnerable to the venous congestion [41]. The T2 hyperintensity may be
reversible after treatment. The differential diagnosis of the T2 hyperintensity would include a superior sagittal sinus
thrombosis with a venous infarction or venous congestion, demyelination, or a dysmyelination and neoplasm [43]. But
the combination of a surplus of pial vessels, T2 hyperintensity deep within the brain, and peripheral enhancement is
highly suggestive of a dural arteriovenous fistula and mandates prompt angiography.

15. Figure 13. CT/MR image correlation of venous congestion. (A) Enhanced CT shows central edema in the left temporal
lobe with tortuous, prominent vessels deep in the sulci (arrows). (B) Proton density weighted MR image shows central
hypointensity (curved arrow) in the left temporal lobe and dilated, tortuous vessels in the sulci (small arrows). (C, D)
Early and late phases of a lateral left occipital artery angiogram shows shunting into the transverse sinus and cortical
venous reflux (closed arrows). Note that the transverse sinus is occluded both proximally and distally (open arrows).
The late phase (D) shows the extent of the venous reflux, both supratentorial and infratentorial.

16. Figure 14. Chronic venous congestion in the temporal/occipital region. (A) Saggital T1-weighted MR image shows
linear hyperintensity (arrow) in the occipital cortex with a central hypointensity. The T1 hyperintensity relates to
infarction from the chronic venous congestion. (B) T2-weighted MR image shows central hyperintensity (curved arrow)
in the temporal/occipital region and tortuous, dilated vessels (closed arrows) on the surface of the brain. (C)
Gadolinium-enhanced MR image better delineates the abnormal vessels (arrows). Note the burr hole (curved arrow)
from the previous biopsy. (D) Lateral distal external carotid artery angiogram shows a shunt into the transverse sinus
(open arrow) which is occluded distally. Note the cortical venous reflux (closed arrows).
At angiography, a delayed circulation time is compatible with venous congestive encephalopathy [44]. This is
analogous to the delayed circulation time seen in the venous congestive myelopathy related to a spinal dural
arteriovenous fistula [45]. Angiography outlines the arterial feeders to the dural arteriovenous fistula, as well as the
venous drainage of the fistula. Often, venous sinus occlusions are evident and contribute to the venous hypertension
and reflux into the cortical or cerebellar veins. Careful scrutiny is needed in the detection of cortical venous reflux.
Global nonselective angiography should be avoided as subtle cortical venous reflux will be missed. Selective,
magnification, subtraction angiography is essential to visualize the cortical venous reflux. A complete assessment of the
cranial circulation is important as 7-8% of patients have multiple dural arteriovenous fistulas [46,47].

17. Figure 15. Hydrocephalus and the PPP. (A) T2-weighted MR image shows dilated lateral ventricles and prominent
flow voids deep in the sulci (arrows). (B, C) Early and late phases of a left occipital artery angiogram shows shunting
into the distal transverse sinus with retrograde flow into an anomalous dural sinus in the parietal region (open arrow)
(B). (C) In the late phase, cortical venous reflux is evident (closed arrows). (D) Late phase of the right internal carotid
artery angiogram shows a PPP in the cerebral hemisphere indicative of venous congestion. (From Willinsky R, Goyal
M, TerBrugge K, et al. Tortuous, engorged pial veins in intracranial dural arteriovenous fistulas: correlations with
presentation, location, and MR findings in 122 patients.
The exact anatomic position of the cortical venous reflux must be clearly defined to allow appropriate treatment
planning. Angiography is critical for the detection of the venous reflux and the assessment of the venous drainage of
the brain. Focal areas of delayed venous drainage in the brain correspond to the site of cortical venous reflux. Often
tortuous, dilated collateral veins develop in the region of the cortical venous reflux. This is in response to the venous
hypertension secondary to the cortical venous reflux. Willinsky et al [44] described this finding of tortuous, dilated,
engorged veins and referred to it as a pseudophlebitic pattern (PPP). PPP is associated with venous rerouting into
dilated transosseous venous channels or retrograde flow into orbital veins. PPP is as a sign of venous congestion of the
brain and may correlate with an aggressive natural history. In their report, no location of a cranial dural
arteriovenous fistula was immune to PPP. Although the presence of PPP is typically concurrent with the existence of
cortical venous reflux , sporadic cases of PPP without cortical venous reflux were found and may be a sign that
correlates with a more aggressive natural history.

18. Figure 16. Venous congestion of the brainstem in a foramen magnum dural arteriovenous fistula with cortical venous
reflux. (A) T2-weighted MR image shows a central hyperintensity in the medulla and a few prominent vessels on the
surface of the brainstem. (B) AP right vertebral artery angiogram shows a shunt at the foramen magnum (open arrow)
with drainage into the anterior spinal vein (closed arrow). (C) Lateral selective angiogram of a dural branch from the
right vertebral artery shows the drainage into the spinal vein (single arrow) and the posterior fossa veins (double
arrow). (D) Post-treatment (embolization and surgery) T2-weighted MR image shows resolution of the congestion.
MANAGEMENT OF CRANIAL DURAL ARTERIOVENOUS FISTULAS
Treatment of dural arteriovenous fistulas is done to improve on the natural history of the disorder. Therefore,
observation should be considered as a completely valid treatment option in patients with dural arteriovenous fistulas
without cortical venous reflux who are tolerating their symptoms. No treatment is especially important in the elderly
patient with a well-tolerated slow-flow fistula of the cavernous sinus without cortical venous reflux. Patients with
cranial dural arteriovenous fistulas without cortical venous reflux have a 98% chance of having a benign course with
no curative treatment, indicating that observation with timely imaging re-evaluation is the best available treatment
[31]. The imaging used in follow-up should include MR with MR angiography. MR angiography with gadolinium may
be more accurate in the assessment of cortical venous reflux and therefore should be helpful for the routine follow-up
of dural arteriovenous fistulas that are being managed conservatively. A 3-year-follow-up angiogram is advised in
patients with stable clinical signs and symptoms. If there is any change in the clinical status, either worsening or
improvement in symptoms, repeat angiography is needed to look for the development of cortical venous reflux or
progressive venous thrombosis and retrograde flow in the dural sinuses.
Intermittent manual carotid compression by the patient has been used by Halbach et al [48] to treat dural
arteriovenous fistulas. The patient is taught to compress the carotid artery with his contralateral hand and stop
compressing if any weakness develops. They report a cure rate of 30% with this technique after 4-6 weeks. This
treatment has been the subject of debate because the 30% cure rate in the short term may reflect the natural history of
the disease.
Endovascular embolization has been demonstrated to be a valid treatment of cranial dural arteriovenous fistulas with
cortical venous reflux [13,49-53]. The same has been demonstrated for surgical therapy [54-58]. It is still a debate
whether total resection or obliteration of the fistula is necessary, or if simple disconnection of the refluxing cortical
veins from the fistula will yield the same result [59]. There are a limited number of reports on the radiosurgical
treatment of cranial dural arteriovenous fistulas [60-63]. In patients with cortical venous reflux , the delayed efficacy
of radiosurgery is not acceptable as the adverse event rate in these patients is 15% per year. Because most cranial
dural arteriovenous fistulas without cortical venous reflux do not need treatment, the risk of radiosurgery in these
patients may not be acceptable, especially in view of the limited data available on the efficacy of this treatment.
Cranial dural arteriovenous fistulas with cortical venous reflux require a multidisciplinary approach to treatment.
Endovascular treatment is often the primary treatment modality. The primary goal of treatment, either endovascular
or surgery, is to eliminate the cortical venous reflux. Complete closure of the fistula is the ideal treatment but not
critical, as eliminating the cortical venous reflux should only be effective in eradicating the risk of intracranial
hemorrhagic or nonhemorrhagic deficits. Endovascular treatment often begins with arterial embolization. The ideal
goal is to occlude the fistula itself which involves reaching the venous side of the fistula. Liquid adhesive agents are the
best agent to permanently occlude a fistula. Particle embolization through the feeding pedicles is satisfactory as a
palliative treatment in dural arteriovenous fistulas without cortical venous reflux or as an adjunct to the definitive
treatment on the venous side, either endovascular or surgical. The endovascular treatment on the venous side is done

19. retrograde through the veins with deposition of coils into the venous compartment at the fistula site. Transvenous
packing of the involved dural sinus is commonly done for transverse sinus and cavernous sinus dural arteriovenous
fistulas with cortical venous reflux. Sacrifice of an involved transverse sinus can only be considered after a thorough
understanding of the venous drainage of the brain. In many of these patients, the brain has developed alternative
pathways for its venous drainage because of the high pressure in the involved venous sinus and/or pre-existing venous
occlusive disease.
Figure 17. Transvenous disconnection of a cavernous dural arteriovenous fistula with cortical venous reflux. (A)
Lateral left external carotid artery angiogram shows shunting into the cavernous sinus (open arrow) and cortical
venous reflux into the sylvian veins (closed arrow). (B) Lateral sphenoparietal venogram (open arrow) shows the
cortical veins that were involved in the fistula. This study was done by a transvenous catheterization through the
inferior petrosal sinus (closed arrow). (C) Radiograph shows the coils that were deposited into the sphenoparietal and
cavernous sinuses. (D) Postembolization lateral external carotid artery angiogram shows that the cortical venous
reflux has been completely eliminated. A small residual fistula (arrow) is seen posteriorly in the cavernous sinus.
Endovascular treatment is indicated for cavernous dural arteriovenous fistulas without cortical venous reflux when
the intraocular pressures cannot be controlled medically. If left untreated, these patients will develop permanent visual
loss. The transvenous femoral approach to the cavernous sinus can be done through the petrosal sinus or, infrequently,
through facial veins. After transvenous coil deposition into the cavernous sinus, there may be worsening of the venous
hypertension in the orbit caused by venous thrombosis within the orbit. This may require oral steroids and anti-
coagulation in order to spare the vision.
Patients with cavernous dural arteriovenous fistulas that are being followed conservatively need careful monitoring by
a neuro-ophthalmologist. Spontaneous venous thrombosis in the orbit may develop in these patients. This results in
worsening of the eye signs and symptoms and raised intraocular pressure. Initially, the raised intraocular pressure
may respond well to topical medical treatment. Patients may require steroids and systemic anticoagulation to save
their vision. The neuro-ophthalmologist can supervise the medical therapy and is the key person to decide if surgical
treatment of the hypertensive glaucoma is needed. Failure of medical therapy is an indication for prompt endovascular
treatment.

20. Surgical treatment may involve one of two strategies. The first strategy is surgical disconnection of the cortical venous
reflux without treating the actual fistula. The second strategy is skeletonization of the involved dural sinus with
interruption of the dural arterial supply and preservation of the cortical veins. Both types of surgical treatment benefit
from preoperative embolization of the arterial feeders. The goal of disconnection alone is to eliminate the future risk of
hemorrhagic or nonhemorrhagic deficits. Disconnection alone will convert a Borden 2 dural arteriovenous fistula to a
Borden 1 dural arteriovenous fistula and thereby favorably alter the natural history. Disconnection alone is often a less
formidable task compared with skeletonization of the involved sinus. Disconnection alone is only feasible when the
cortical venous reflux is anatomically limited to a limited area. Skeletonization of the dural sinus requires a large
operation as the entire dural sinus must be isolated from its dural arterial supply.
SUMMARY
SUMMARY
Cranial dural arteriovenous fistulas present with a wide spectrum of clinical findings from pulsatile tinnitus alone to
intracranial hemorrhage and Nonhemorrhagic neurologic deficits. The neurologic sequelae are a consequence of
venous hypertension and venous congestion. dural arteriovenous fistulas with cortical venous reflux can present with
or develop a venous congestive encephalopathy that can be recognized on MR imaging as a diffuse T2 hyperintensity
in the deep white matter of the cerebral or cerebellar hemispheres. The T2 hyperintensity has a characteristic
peripheral enhancement. The telltale sign on MR imaging is the plethora of prominent pial vessels on the surface of the
brain that are the engorged cortical veins participating in the cortical venous reflux. Selective angiography is critical
for the accurate assessment of the cortical venous reflux. dural arteriovenous fistulas with cortical venous reflux
require prompt treatment, either endovascular alone or a combination of endovascular treatment and surgery.
Addendum

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REFERENCES
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