Arteriovenous Fistula

Overview

Arteriovenous fistulas (AVFs) are direct pathologic arteriovenous shunts representing 10-15% of all cerebrovascular malformations with AV shunting. The prototypical AVF is an acquired lesion between transosseous-extracranial and/or meningeal arteries into the wall of a thrombosed dural venous sinus compromising a dural AVF (DAVF) and resulting in hypertensive venous congestion and venopathy, however pathologic arteriovenous fistulous connections may exist along any dural margin, sinus, or venous tributary.

DAVFs are distinguished from pial-parenchymal arteriovenous malformations by the predominance of dural arterial supply and the absence of a parenchymal nidus, however AVMs may have pial or dural fistulous components. The majority of DAVFs present in adulthood and are most commonly located at the transverse-sigmoid sinus wall. Clinical presentation and imaging findings are highly variable depending on anatomic site, degree of AV shunting, and venous reflux.

Transverse-sigmoid sinus DAVFs typically present with pulsatile tinnitus. DAVFs may present with encephalopathic symptoms secondary to venous hypertension, ischemia, and/or thrombosis. DAVFs with deep/inferior drainage to the petrosal sinuses and perimedullary venous plexus may result in progressive myelopathy and central respiratory failure.

Congenital arteriovenous fistulas, including DAVF, Vein of Galen Aneurysmal Malformations (VGAM) of the subarachnoid space, and non-galenic pial AVF (pAVF) encountered in the pediatric population, have unique developmental and pathophysiologic characteristics and tend to be very rare. Like AVMs, underlying parenchymal abnormalities have been hypothesized to result from vascular steal phenomenon and venous congestion. Infants with large congenital DAVF, VGAM, and non-galenic pAVFs can present with congestive heart failure (early) and developmental delay or increased head circumference (late).

Carotid Cavernous Fistulas (CCF), included in this category, represent pathologic shunts between the cavernous ICA and the cavernous sinus, resulting in unique symptomology typically with pulsatile exophthalmos and cranial neuropathies of III, IV, and VI.

Dural Arteriovenous Fistula (DAVF)

Figure 1: 63-year-old male with tinnitus and headache. Top row: axial CT image demonstrates focal permeative osseous lucency adjacent to the right adjacent to the right transverse-sigmoid sinus junction. Axial T1 post contrast image demonstrates abnormally increased dural enhancement adjacent to the right transverse-sigmoid sinus junction. Bottom row: MRA MIP image reveals abnormal flow-related enhancement of numerous transosseous vessels converging at the right transverse-sigmoid sinus junction wall. DSA confirms a right transverse-sigmoid sinus junction DAVF, Cognard type I (white arrows) with arterial supply primarily by branches of the distal right occipital artery, minor contribution by the posterior branch of the right middle meningeal artery, and antegrade venous drainage directly from the right transverse-sigmoid sinus junction.

Imaging

General features
- Intracranial DAVFs present with a range of symptomatology which correlates with both anatomic location and regional venous drainage pattern (Cognard classification). Cross-sectional imaging features are often subtle, missed, or misinterpreted. DAVFs can involve any dural venous sinus, most commonly the transverse-sigmoid sinus junction (35-40%) and less commonly the superior sagittal sinus and superior petrosal sinus.
CT
- NECT
  - Commonly normal, unremarkable study
  - Hyperdense dural sinus (thrombosis) may be identified
  - Dilated transosseous calvarial vascular channels with associated permeative, erosive changes can be seen in some cases, generally long-standing lesions
  - Enlargement of the foramen spinosum (hypertrophy of the transmitted middle meningeal artery)
  - Sensitive for parenchymal and subarachnoid hemorrhage in acute rupture of DAVF (more common than subdural hemorrhage) or flow-related aneurysm (rare)
  - In contrast to pial AVMs which typically demonstrate parenchymal hematomas and/or IVH (occasionally-to-rarely SAH)
  - Relatively sensitive for parenchymal ischemia and edema, though evaluation is limited in the posterior fossa as is the case in other disease entities
CT Angiography:
- Serpiginous, dilated, and hypertrophied arterial feeders closely apposed to dural surfaces and dural venous sinuses
- Dilated draining veins and varices (common), flow-related aneurysms (rare)
- Dural sinus stenosis and/or thrombosis
- Dilated, tortuous cortical draining veins in higher Cognard grade lesions
- Pitfalls
  - As there is absence of nidus, direct visualization of isodense to hyperdense serpiginous structures related to hypertrophied feeding arteries and draining veins are likely to be only appreciated in restrospect (if at all)
  - If there is evidence of rupture and hemorrhage, proceed to contrast-enhanced study
MRI
- General Features
  - Absence of parenchymal nidus tangle of serpiginous flow voids
  - High flow fistulas may demonstrate anomalous flow-related phenomena
  - Increased number of flow voids
  - Increased size of flow voids
  - Abnormal locations related to venous congestion
    - Prominent transosseous/meningeal vessels
    - Prominent cortical veins
  - Excellent sensitivity and specificity for detection and staging of blood products related to associated hemorrhage
- T2, FLAIR
  - May reveal parenchymal hyperintensity related to gliosis and/or venous congestion
  - Seen in higher grade lesions due to abnormal retrograde leptomeningeal/cortical venous reflux (can be striking)
- T2*, GRE, SWI
  - Signal loss (blooming) of thrombosed dural sinuses
- DWI
  - Typically normal
  - May reveal venous infarct/ischemia if present
- Postcontrast imaging
  - Variable dural sinus wall contrast enhancement
  - Abnormally increased leptomeningeal enhancement
- MR Angiography
  - MRA/MRV should generally be considered complementary to conventional MRI
  - 3D phase-contrast MRA with low velocity encoding can identify AV fistula components
    - Feeding arteries
    - Flow reversal in draining veins
  - Time-resolved contrast-enhanced MRA and MRV proves useful in estimating angiographic dynamics such as flow reversal in draining veins when present
    - Feeding arteries are often easy to identify (because of location and dilatation)
    - Draining veins can be identified by their larger caliber relative to arteries and drainage into deep or cortical veins
    - Dilated, tortuous cortical draining veins in higher Cognard grade lesions
    - MRV demonstrates occluded parent sinus and collateral flow
- Pitfalls
  - Sigmoid Sinus-Jugular Foramen Pseudolesion
    - Slow or asymmetric flow creates variable signal on MR sequences
    - Use MRV with multiple encoding gradients to clarify
  - Thrombosed Dural Sinus
    - Congested venous collateralization drainage can mimic DAVF, without arterial shunt
    - Evaluate all dural margins as well as close attention to the overlying scalp
  - Limitations
    - Prone to multitude of artifacts that can be both helpful and difficult to interpret
      - Pulsation artifacts may be seen with DAVFs
      - Pulsation artifacts become more pronounced on T1 spin-echo contrast-enhanced images but not on IRSPGR contrast-enhanced images
    - Generally less cost-effective, less availability
    - CT is more easily performed in uncooperative, combative patients
Digital Subtraction Angiography
- Angioarchitecture characterization
- Important to completely evaluate bilateral ECA, ICA, and vertebrobasilar arteries to completely characterize arterial supply
  - Multiple arterial feeders are typical, can have bilateral arterial supply
  - Predominant supply from meningeal arteries
    - Dural and transosseous branches from ECA (commonly the occipital and middle meningeal arteries)
    - Tentorial and dural branches from ICA and VA
    - Parasitization of pial arteries (i.e. ACA, MCA, PCA and tributaries) with larger DAVFs
  - Arterial inflow into parallel recipient venous pouch
  - Venous drainage pattern
    - Antegrade flow
    - Retrograde flow into cortical veins and/or spinal perimedullary veins
- Staging, Grading, & Classification
  - Cognard classification of intracranial DAVFs
    - Correlates venous drainage pattern with risk of ICH
      - Grade 1: Located in sinus wall, normal antegrade venous drainage, benign clinical course
      - Grade 2A: Located in main sinus, reflux into sinus but not cortical veins
      - Grade 2B: Reflux (retrograde drainage) into cortical veins (10-20% hemorrhage rate)
      - Grade 3: Direct cortical venous drainage, no venous ectasia (40% hemorrhage)
      - Grade 4: Direct cortical venous drainage, venous ectasia (65% hemorrhage)
      - Grade 5: Spinal perimedullary venous drainage, progressive myelopathy
    - Prognosis and clinical course depends on location and venous drainage pattern
    - 98% of DAVFs without retrograde venous drainage have benign course
    - DAVFs with retrograde venous drainage have aggressive clinical course and are more likely to result in parenchymal hemorrhage

Figure 2: Right superior petrosal sinus DAVF, Cognard IIa+b. Top row: Sagittal T1W MRI (left), CTA 3D-reconstruction image (middle), and Sagittal CTA MIP reconstruction (right image) demonstrate focal dilated vessels (arrows). DSA (bottom row) confirms a right superior petrosal sinus DAVF, Cognard IIa+b (arrows) with arterial supply from the petrosquamosal division of the right middle meningeal artery via the basal tentorial artery as well as transosseous occipital branches and to a lesser extent by temporal branches of the middle meningeal artery. Venous drainage is into a prominent venous pouch with subsequent drainage into the superior petrosal sinus, petrosal vein and basal vein of Rosenthal.

Carotid-Cavernous Fistula (CCF)

Figure 3: Carotid-Cavernous Fistula. Top row: Axial CT images demonstrate suspected dilatation of the superior ophthalmic vein (arrows) and proptosis of the right globe (arrow). Middle row: Axial T1W postcontrast MRI demonstrates bulging of the right cavernous sinus (white arrow). Coronal T1W MRI illustrates the marked, asymmetric enlargement of the right superior ophthalmic vein (black arrow). Bottom row: DSA, right ICA injection confirms a Type A direct carotid-cavernous fistula (white arrows) with venous drainage primarily into the ophthalmic venous system, clival venous plexus, and contralateral inferior petrosal sinus.

Imaging

General features
- Pathologic shunts between the cavernous ICA and the cavernous sinus
- Barrow classification based on angiographic characterization of arterial supply
  - Type A: Direct ICA-cavernous sinus high-flow shunt (not DAVF)
  - Type B: Dural ICA branches-cavernous shunt
  - Type C: Dural ECA-cavernous shunt
  - Type D: ECA and ICA dural branches shunt to cavernous sinus
- Natural history of CCF is variable
  - Spectrum: spontaneous closure to rapid symptom progression
  - Direct CCF
    - have a relatively high spontaneous rate (~8%) of hemorrhage (SAH, ICH, or epistaxis). Subconjunctival hemorrhage is also common.
  - Indirect CCF
    - Indicators of poor outcome include feeding vessel aneurysms and, like other dural-based AV shunts, there is increased risk of hemorrhage if retrograde cortical venous reflux develops.
Cross-sectional imaging findings (CT and MRI)
- Asymmetric subtle mass effect of the cavernous sinus
- Asymmetric early enhancement of the cavernous sinus
- Asymmetric enlargement of the ipsilateral superior ophthalmic vein
- Asymmetric ipsilateral proptosis, extraocular muscle enlargement
- Increased number of vessels (ie. flow voids) in the cavernous sinus

For more information, please see the corresponding chapter in Radiopaedia.

Contributor: Daniel Murph, MD

DOI: https://doi.org/10.18791/nsatlas.v2.03.03.04.03

References

Berenstein A, Lasjaunias, P. Surgical Neuroangiography, Vol 3. Clinical and Interventional Aspects in Children Springer-Verlag, New York, 1992.

Brown RD Jr, Flemming KD, Meyer FB, et al. Natural history, evaluation, and management of intracranial vascular malformations. Mayo Clin Proc 2005;80(2): 269–81.

Chaudhary MY, Sachdev VP, Cho SH, et al. Dural arteriovenous malformation of the major venous sinuses: an acquired lesion. AJNR Am J Neuroradiol 1982;3(1):13–9.

Chew J et al: Arterial Onyx embolisation of intracranial DAVFs with cortical venous drainage. Can J Neurol Sci. 36(2):168-75, 2009

Chung SJ, Kim JS, Kim JC, et al. Intracranial dural arteriovenous fistulas: analysis of 60 patients. Cerebrovasc Dis 2002;13(2):79–88.

Cognard C, Casasco A, Toevi M, et al. Dural arteriovenous fistulas as a cause of intracranial hypertension due to impairment of cranial venous outflow. J Neurol Neurosurg Psychiatry 1998;65(3):308–16.

Cognard C, Gobin YP, Pierot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 1995;194(3):671–80.

Davies MA, TerBrugge K, Willinsky R, et al. The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 1996;85(5):830–7.

Farb RI et al: Cranial Dural Arteriovenous Fistula: Diagnosis and Classification with Time-Resolved MR Angiography at 3T. AJNR Am J Neuroradiol. Epub ahead of print, 2009

Hashiguchi A, Mimata C, Ichimura H, et al. Venous aneurysm development associated with a dural arteriovenous fistula of the anterior cranial fossa with devastating hemorrhage–case report. Neurol Med Chir (Tokyo) 2007;47(2):70–3.

Hasumi T, Fukushima T, Haisa T, et al. Focal dural arteriovenous fistula (DAVF) presenting with progressive cognitive impairment including amnesia and alexia. Intern Med 2007;46(16):1317–20.

Hetts SW, et al. Pediatric intracranial dural arteriovenous fistulas: age-related differences in clinical features, angioarchitecture, and treatment outcomes. J neurosurg Pediatr Volume 18 • November 2016

Hirono N, Yamadori A, Komiyama M. Dural arteriovenous fistula: a cause of hypoperfusion-induced intellectual impairment. Eur Neurol 1993;33(1):5–8.

Kim MS, Han DH, Kwon OK, et al. Clinical characteristics of dural arteriovenous fistula. J Clin Neurosci 2002;9(2):147–55.

Kincaid P, Duckwiler GR, Gobin YP, Vinuela F. Dural arteriovenous fistula in children: endovascular treatment and outcomes in seven cases. AJNR 2001; 22: 1217–1225.

Lagares A, Perez-Nunez A, Alday R, et al. Dural arteriovenous fistula presenting as brainstem ischaemia. Acta Neurochir (Wien) 2007;149(9): 965–7.

Lasjaunias P, Chiu M, TerBrugge K, et al. Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 1986;64(5):724–30.

Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 1969;93(5):1071–8.

Ratlif J, Voorhies RM. Arteriovenous fistula with associated aneurysms coexisting with dural arteriovenous malformation of the anterior inferior falx. J Neurosurg 199; 91: 303–307.

van Dijk JM, TerBrugge KG, Willinsky RA, et al. Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke 2002;33(5):1233–6.