The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas

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✓ A number of classification schemes for intracranial dural arteriovenous fistulas (AVFs) have been published that claim to predict which lesions will present in a benign or aggressive fashion based on radiological anatomy. We have tested the validity of two proposed classification schemes for the first time in a large single-institution study.

A series of 102 intracranial dural AVFs in 98 patients assessed at a single institution was analyzed. All patients were classified according to two grading scales: the more descriptive schema of Cognard, et al. (Cognard) and that recently proposed by Borden, et al. (Borden). According to the Borden classification, 55 patients were Type I, 18 Type II, and 29 Type III. Using the Cognard classification, 40 patients were Type I, 15 Type IIA, eight Type IIB, 10 Type IIA+B, 13 Type III, 12 Type IV, and four Type V.

Intracranial hemorrhage (ICH) or nonhemorrhagic neurological deficit was considered an aggressive presenting clinical feature. A total of 16 (16%) of 102 intracranial dural AVFs presented with hemorrhage. Eleven of these hemorrhages (69%) occurred in either anterior cranial fossa or tentorial lesions. When analyzed according to the Borden classification, none (0%) of 55 Type I intracranial dural AVFs, two (11%) of 18 Type II, and 14 (48%) of 29 Type III intracranial dural AVFs presented with hemorrhage (p < 0.0001). After exclusion of visual or cranial nerve deficits that were clearly related to cavernous sinus intracranial dural AVFs, nonhemorrhagic neurological deficits were a feature of presentation in one (2%) of 55 Type I, five (28%) of 18 Type II, and nine (31%) of 29 Type III patients (p < 0.0001). When combined, an aggressive clinical presentation (ICH or nonhemorrhagic neurological deficit) was seen most commonly in intracranial dural AVFs located in the tentorium (11 (79%) of 14) and the anterior cranial fossa (three (75%) of four), but this simply reflected the number of higher grade lesions in these locations. Aggressive clinical presentation strongly correlated with Borden types: one (2%) of 55 Type I, seven (39%) of 18 Type II, and 23 (79%) of 29 Type III patients (p < 0.0001). A similar correlation with aggressive presentation was seen with the Cognard classification: none (0%) of 40 Type I, one (7%) of 15 Type IIA, three (38%) of eight Type IIB, four (40%) of 10 Type IIA+B, nine (69%) of 13 Type III, 10 (83%) of 12 Type IV, and four (100%) of four Type V (p < 0.0001).

No location is immune from harboring lesions capable of an aggressive presentation. Location itself only raises the index of suspicion for dangerous venous anatomy in some intracranial dural AVFs. The configuration of venous anatomy as reflected by both the Cognard and Borden classifications strongly predicts intracranial dural AVFs that will present with ICH or nonhemorrhagic neurological deficit.

Article Information

Address reprint requests to: M. Christopher Wallace, M.D., F.R.C.S.(C), Division of Neurosurgery, The Toronto Hospital—Western Division, 399 Bathurst Street, Toronto, Ontario, Canada, M5T 2S8.

© AANS, except where prohibited by US copyright law.

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    Stylized artist's representations of standard left transverse sinus (TS) intracranial dural arteriovenous fistulas (AVFs) of different types compared with same type cerebral angiographic images. The artist's images illustrate the nidus in the wall of the TS, which is opened longitudinally to reveal the varying content of arterial (red) and venous (blue) blood to suggest flow patterns. Dural arteries within the convexity dura are seen coursing to supply the nidus. A window in the dura above the TS has been opened to reveal the occipital lobe being retracted to expose a feeding artery within the tentorial dura and a leptomeningeal vein coursing from the brain to the TS. A and B: Borden Type I/Cognard Type I intracranial dural AVF, which drains into meningeal vein(s) or dural venous sinus (DVS), with anterograde DVS flow. Artist's rendering (A) displaying well-oxygenated blood (red) exiting the nidus as it mixes with the normal anterograde flow (blue) in the TS. There is no retrograde leptomeningeal venous drainage. Selective right occipital artery (arrow) angiogram, lateral projection (B) demonstrating a diffuse TS nidus that drains anterogradely into the TS and sigmoid sinus (arrowheads). C and D: Borden Type I/Cognard Type IIA intracranial dural AVF draining into the meningeal vein(s) or DVS with retrograde DVS flow. Artist's rendering (C) demonstrating retrograde DVS flow (red blood exiting the nidus fills the TS). There is no retrograde leptomeningeal venous drainage. Left distal external carotid artery angiogram, lateral projection (D), showing middle meningeal (arrowhead) branches feeding a TS nidus. Only a retrograde flow is seen in the TS (arrow)yy. E and F: Borden Type II/Cognard Type IIB intracranial dural AVF exhibiting retrograde leptomeningeal venous drainage as well as drainage into the meningeal vein(s) or DVS with anterograde DVS flow. Artist's rendering (E) displaying nidal outflow (red) as it mixes with the normal anterograde TS flow (blue). A leptomeningeal vein (now red) is also involved in the lesion's venous drainage (retrograde leptomeningeal venous drainage). Right external carotid artery (large arrow) angiogram, lateral projection (F) of a cavernous sinus intracranial dural AVF with retrograde leptomeningeal venous drainage into the cortical veins (arrowheads) and anterograde flow through the inferior petrosal sinus (open arrow). Reflux into the superior ophthalmic vein (small arrow) is seen. G and H: Borden Type II/Cognard Type IIA+B intracranial dural AVF displaying retrograde leptomeningeal venous drainage, but also drainage into meningeal vein(s) or DVS with retrograde DVS flow. Artist's rendering (G) demonstrating retrograde DVS flow (red blood filling the TS). In addition, there is retrograde leptomeningeal venous drainage (red leptomeningeal vein). Selective right occipital artery (small straight arrow) angiogram, lateral projection (H), showing a TS nidus that drains anterogradely through the transverse/sigmoid sinuses (arrowheads). The intracranial dural AVF also has retrograde DVS flow into the superior sagittal (curved black arrow) and straight (open arrow) sinuses. The retrograde leptomeningeal venous drainage into the deep venous system is seen (large straight arrow). I and J: Borden Type III/Cognard Type III intracranial dural AVF showing retrograde leptomeningeal venous drainage only. Artist's rendering (I) depicting nidal outflow that uses leptomeningeal veins exclusively (red). The TS (blue) may be occluded or works in isolation carrying venous blood. Selective left occipital artery (arrow) angiogram, lateral projection (J) showing a TS (arrowhead) intracranial dural AVF. Outflow occurs via leptomeningeal veins such as the vein of Labbé (curved arrow). The segment of TS is isolated (open arrows). K and L: Borden Type III/Cognard Type IV intracranial dural AVF exhibiting retrograde leptomeningeal venous drainage (with ectasia) only. Artist's rendering (K) similar to that shown in I, but illustrating an ectatic leptomeningeal vein. Right external carotid artery angiogram, lateral projection (L) in which a large posterior middle meningeal branch (small arrow) is seen to supply a TS nidus (large arrow) that empties exclusively into the vein of Labbé (curved arrow). Blood ultimately escapes via other cortical veins, including an ectatic sylvian vein (arrowhead) on the way to the cavernous sinus. M: Borden Type III/Cognard Type V intracranial dural AVF, shown in selective right ascending pharyngeal artery (arrowhead) angiogram, lateral projection, displaying retrograde leptomeningeal venous drainage with involvement of perimedullary spinal veins. This foramen magnum intracranial dural AVF (thin arrow) has retrograde leptomeningeal venous drainage into a dorsal perimedullary spinal vein (large arrow).

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    Contrast-enhanced T1-weighted axial magnetic resonance images demonstrating contrast enhancement in the territory of leptomeningeal veins in the deep system subjected to retrograde flow from an intracranial dural arteriovenous fistula. Left: Dorsal midbrain (arrow). Right: Right thalamus (arrow).

References

  • 1.

    Aminoff MJ: Vascular anomalies in the intracranial dura mater. Brain 96:6016121973Aminoff MJ: Vascular anomalies in the intracranial dura mater. Brain 96:601–612 1973

    • Search Google Scholar
    • Export Citation
  • 2.

    Awad IALittle JRAkrawi WPet al: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:8398501990Awad IA Little JR Akrawi WP et al: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:839–850 1990

    • Search Google Scholar
    • Export Citation
  • 3.

    Barnwell SLHalbach VVDowd CFet al: A variant of arteriovenous fistulas within the wall of dural sinuses. Results of combined surgical and endovascular therapy. J Neurosurg 74:1992041991Barnwell SL Halbach VV Dowd CF et al: A variant of arteriovenous fistulas within the wall of dural sinuses. Results of combined surgical and endovascular therapy. J Neurosurg 74:199–204 1991

    • Search Google Scholar
    • Export Citation
  • 4.

    Borden JAWu JKShucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:1661791995Borden JA Wu JK Shucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:166–179 1995

    • Search Google Scholar
    • Export Citation
  • 5.

    Castaigne PBories JBrunet Pet al: Les fistules artérioveineuses méningées pures à drainage veineux cortical. Rev Neurol 132:1691811976Castaigne P Bories J Brunet P et al: Les fistules artérioveineuses méningées pures à drainage veineux cortical. Rev Neurol 132:169–181 1976

    • Search Google Scholar
    • Export Citation
  • 6.

    Cognard CGobin YPPierot Let al: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194:6716801995Cognard C Gobin YP Pierot L et al: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194:671–680 1995

    • Search Google Scholar
    • Export Citation
  • 7.

    Djindjian RMerland JJTheron J: Super-Selective Arteriography of the External Carotid Artery. New York: Springer-Verlag1977 pp 606628Djindjian R Merland JJ Theron J: Super-Selective Arteriography of the External Carotid Artery. New York: Springer-Verlag 1977 pp 606–628

    • Search Google Scholar
    • Export Citation
  • 8.

    Fermand MReizine DMelki JPet al: Long term follow-up of 43 pure dural arteriovenous fistulae (AVF) of the lateral sinus. Neuroradiology 29:3483531987Fermand M Reizine D Melki JP et al: Long term follow-up of 43 pure dural arteriovenous fistulae (AVF) of the lateral sinus. Neuroradiology 29:348–353 1987

    • Search Google Scholar
    • Export Citation
  • 9.

    Houser OWBaker HL JrRhoton AL Jret al: Intracranial dural arteriovenous malformations. Radiology 105:55641972Houser OW Baker HL Jr Rhoton AL Jr et al: Intracranial dural arteriovenous malformations. Radiology 105:55–64 1972

    • Search Google Scholar
    • Export Citation
  • 10.

    Kosnik EJHunt WEMiller CA: Dural arteriovenous malformations. J Neurosurg 40:3223291974Kosnik EJ Hunt WE Miller CA: Dural arteriovenous malformations. J Neurosurg 40:322–329 1974

    • Search Google Scholar
    • Export Citation
  • 11.

    Lalwani AKDowd CFHalbach VV: Grading venous restrictive disease in patients with dural arteriovenous fistulas of the transverse/sigmoid sinus. J Neurosurg 79:11151993Lalwani AK Dowd CF Halbach VV: Grading venous restrictive disease in patients with dural arteriovenous fistulas of the transverse/sigmoid sinus. J Neurosurg 79:11–15 1993

    • Search Google Scholar
    • Export Citation
  • 12.

    Lamas ELobato RDEsparza Jet al: Dural posterior fossa AVM producing raised sagittal sinus pressure. Case report. J Neurosurg 46:8048101977Lamas E Lobato RD Esparza J et al: Dural posterior fossa AVM producing raised sagittal sinus pressure. Case report. J Neurosurg 46:804–810 1977

    • Search Google Scholar
    • Export Citation
  • 13.

    Lasjaunias PChiu MTer Brugge Ket al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:7247301986Lasjaunias P Chiu M Ter Brugge K et al: Neurological manifestations of intracranial dural arteriovenous malformations. J Neurosurg 64:724–730 1986

    • Search Google Scholar
    • Export Citation
  • 14.

    Malik GMPearce JEAusman JIet al: Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery 15:3323391984Malik GM Pearce JE Ausman JI et al: Dural arteriovenous malformations and intracranial hemorrhage. Neurosurgery 15:332–339 1984

    • Search Google Scholar
    • Export Citation
  • 15.

    Newton THCronqvist S: Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 93:107110781969Newton TH Cronqvist S: Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 93:1071–1078 1969

    • Search Google Scholar
    • Export Citation
  • 16.

    Obrador SUrquiza P: Angioma arteriovenoso de la tienda del cerebelo. Rev Esp Oto-Neuro-Oftalmol Neurochir 10:3873921951Obrador S Urquiza P: Angioma arteriovenoso de la tienda del cerebelo. Rev Esp Oto-Neuro-Oftalmol Neurochir 10:387–392 1951

    • Search Google Scholar
    • Export Citation
  • 17.

    Tomsick TTew JLukin R: Intracranial arteriovenous malformations with increased intracranial pressure: response to immobilization in Smith RRHaerer AFRussel WF (eds): Vascular Malformations and Fistulas of the Brain. New York: Raven Press1982 pp 119127Tomsick T Tew J Lukin R: Intracranial arteriovenous malformations with increased intracranial pressure: response to immobilization in Smith RR Haerer AF Russel WF (eds): Vascular Malformations and Fistulas of the Brain. New York: Raven Press 1982 pp 119–127

    • Search Google Scholar
    • Export Citation
  • 18.

    Willinsky RTerbrugge KMontanera Wet al: Venous congestion: an MR finding in dural arteriovenous malformations with cortical venous drainage. AJNR 15:150115071994Willinsky R Terbrugge K Montanera W et al: Venous congestion: an MR finding in dural arteriovenous malformations with cortical venous drainage. AJNR 15:1501–1507 1994

    • Search Google Scholar
    • Export Citation

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