Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course

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✓ The natural history of cranial dural arteriovenous malformations (AVM's) is highly variable. The authors present their clinical experience with 17 dural AVM's in adults, including 10 cases with an aggressive neurological course (strictly defined as hemorrhage or progressive focal neurological deficit other than ophthalmoplegia). Two of these 10 patients died prior to surgical intervention and a third was severely disabled by intracerebral hemorrhage. Six patients underwent surgical resection of their dural AVM, with preparatory embolization in two cases. One patient received embolization and radiation therapy without surgery. Six of the seven cases without an aggressive neurological course were treated conservatively, and the seventh patient underwent embolization of a cavernous sinus dural AVM because of worsening ophthalmoplegia. In order to clarify features associated with aggressive behavior, a comprehensive meta-analysis was performed on 360 additional dural AVM's reported in the literature with sufficiently detailed clinical and angiographic information. The location and angiographic features of 100 aggressive cases were compared to those of 277 benign cases. No location of dural AVM's was immune from aggressive neurological behavior; however, an aggressive neurological course was least often associated with cases involving the transverse-sigmoid sinuses and cavernous sinus and most often associated with cases at the tentorial incisura. Contralateral contribution to arterial supply and rate of shunting (high vs. low flow) did not correlate with aggressive neurological behavior as defined. Leptomeningeal venous drainage, variceal or aneurysmal venous dilations, and galenic drainage correlated significantly (p < 0.05) with aggressive neurological presentation. The latter three angiographic features often coexisted in the same dural AVM. It is concluded that these features significantly increase the natural risk of dural AVM's, and warrant a more vigilant therapeutic strategy.

Abstract

✓ The natural history of cranial dural arteriovenous malformations (AVM's) is highly variable. The authors present their clinical experience with 17 dural AVM's in adults, including 10 cases with an aggressive neurological course (strictly defined as hemorrhage or progressive focal neurological deficit other than ophthalmoplegia). Two of these 10 patients died prior to surgical intervention and a third was severely disabled by intracerebral hemorrhage. Six patients underwent surgical resection of their dural AVM, with preparatory embolization in two cases. One patient received embolization and radiation therapy without surgery. Six of the seven cases without an aggressive neurological course were treated conservatively, and the seventh patient underwent embolization of a cavernous sinus dural AVM because of worsening ophthalmoplegia. In order to clarify features associated with aggressive behavior, a comprehensive meta-analysis was performed on 360 additional dural AVM's reported in the literature with sufficiently detailed clinical and angiographic information. The location and angiographic features of 100 aggressive cases were compared to those of 277 benign cases. No location of dural AVM's was immune from aggressive neurological behavior; however, an aggressive neurological course was least often associated with cases involving the transverse-sigmoid sinuses and cavernous sinus and most often associated with cases at the tentorial incisura. Contralateral contribution to arterial supply and rate of shunting (high vs. low flow) did not correlate with aggressive neurological behavior as defined. Leptomeningeal venous drainage, variceal or aneurysmal venous dilations, and galenic drainage correlated significantly (p < 0.05) with aggressive neurological presentation. The latter three angiographic features often coexisted in the same dural AVM. It is concluded that these features significantly increase the natural risk of dural AVM's, and warrant a more vigilant therapeutic strategy.

Cranial dural arteriovenous malformations (AVM's) consist of a nidus of arteriovenous shunting within the dura mater. This nidus is often in the proximity of a dural sinus which may be narrowed or obstructed. Arterial supply is recruited from dural arteries and from pachymeningeal branches of cerebral arteries. Venous drainage is through the dural sinus and/or other dural and leptomeningeal venous channels. Retrograde leptomeningeal venous drainage is often tortuous, variceal, or frankly aneurysmal.

The natural history of dural AVM's is highly variable. Spontaneous regression or thrombosis is not uncommon,7,33,61,81 and patients may have no symptoms or benign symptomatology for many years.3,8,16,20,79 A small group of cases can exhibit aggressive neurological behavior.17,19,21,24,35,41,56,63,111 We report our clinical experience with 17 dural AVM's, including 10 cases with hemorrhagic or nonhemorrhagic stroke. In addition, we present a comprehensive meta-analysis of the literature with comparison of angiographic features of aggressive and nonaggressive cases. For the purpose of this study, aggressive neurological behavior is defined as hemorrhage or progressive focal neurological deficit other than ophthalmoplegia. Dural AVM's associated with papilledema or increased intracranial pressure alone are considered with nonaggressive lesions, but are analyzed separately.

Clinical Material and Methods

Between January, 1986, and December, 1988, the senior authors (I.A.A. and J.R.L.) cared for 17 adults with dural AVM's. Five of these were managed by I.A.A. at two institutions other than the Cleveland Clinic Foundation, and 12 cases were treated by I.A.A. or J.R.L. at the Cleveland Clinic Foundation. These 12 cases represented all dural AVM's managed at that institution during the 3-year study period. Of these 12 cases, three were referred with angiograms performed elsewhere. The remaining nine cases accounted for 20% of 45 AVM's identified on 797 consecutive cerebral angiograms. Infantile cases with vein of Galen fistulae were excluded from this series.

Aggressive Cases

Table 1 summarizes the clinical and angiographic features of the 10 patients with an aggressive neurological course. There were five women and five men, with a mean age of 57.3 years (range 39 to 78 years). Mean duration of symptoms prior to the first aggressive neurological event was 5.6 years (range 0 to 23 years). The presenting event was a hemorrhagic stroke in eight cases, a nonhemorrhagic brain-stem stroke in one case, and a hemorrhage following progressive nonhemorrhagic brain-stem dysfunction in one case. In one instance, the presence of bilateral middle cerebral artery aneurysms prevented a definite determination as to whether the dural AVM was the source of hemorrhage; however, clear evidence of previous bleeding in the region of the dural AVM was found at surgery. The dural AVM was located at the tentorial incisura in four cases, at the transverse sinus in two, at the anterior falx (base of the anterior cranial fossa) in one, at the mid-portion of the superior sagittal sinus in one, at the middle cranial fossa in one, and at the tentorial incisura and transverse sinus in one.

TABLE 1

Clinical and angiographic features of 10 patients with aggressive dural AVM's*

Case No.Age (yrs), SexHistoryClinical PresentationDural AVM LocationArterial SupplyVenous DrainageTreatmentOutcome & Follow-Up Period
160, Ftrauma to face at age 6 yrs, syncope at age 26 yrs, pulsatile tinnitus for 23 yrsmassive cerebral hemorrhage (? related to low-dose anticoagulants received for pulmonary embolism) with deep comalt middle fossabilat ICA & ECA branches, high flowcortical venous drainage to superior sagittal sinussupportivedied
278, Fpulsatile tinnitus for 12 yrsmassive cerebellar & ventricular hemorrhage with deep comaTransverse sinusoccipital & tentorial arteries (bilat), high flowcerebellar & cortical veins, large vermian venous aneurysmsupportivedied
359, M1 yr progressive rostral brain-stem dysfunctionbrain-stem stroke, lt temporal lobe hemorrhage following meningeal biopsy (to rule out basal meningeal process)tentorial & transverse sinuslt occipital & tentorial arteries (unilat), high flowgalenic drainage without varices, sigmoid sinus occlusionembolization, supportivesevere disability from hemorrhage
453, Fpulsatile tinnitus for 2 yrsacute onset of partial Weber syndrometentorial incisuraipsilateral tentorial & occipital arteries, low flowgalenic, variceal prepontine veinsembolization of ECA feeders, subtemporal excision of nidus, no residualasymptomatic, 30 mos
549, Frepeated cerebral & scalp vessel hemorrhages for 33 yrsnew facial vessel hemorrhageface & middle fossabilat ECA's and ICA's, high flowgalenic & transverse sinus, multiple variceal veins in suprasellar & interpeduncular cisternsembolization, radiation therapyno new symptoms, 24 mos
661, Macute thalamic & ventricular hemorrhagetentorial incisurart PCA, SCA, tentorial branches, & meningeal ECA branches, low flowgalenic, large venous aneurysmsurgical excision, small residual nidusasymptomatic, 24 mos
743, Msubarachnoid hemorrhageanterior falxbilat ethmoidal arteries, ECA scalp & meningeal arteries, high flowleft middle cerebral vein via giant venous varicesresection of nidus at base of falx, disconnection of bridging veins, no residualno new symptoms, 38 mos
861, Fpulsatile tinnitus for 12 yrs, partial embolization at age 50 yrsacute rt temporal hemorrhagert transverse sinusboth ICA, vertebral, ECA scalp, & meningeal branches, very high flowtransverse sinus, cortical cerebral & cerebellar veins, multiple varicesmultiple embolizations followed by excision, no residualasymptomatic, 30 mos
939, Mconcussion at age 37 yrsacute intraventricular, hemorrhage & comaupper dural convexity (lt frontoparietal)bilat ECA scalp & meningeal branches, low flowsuperior sagittal sinus, single cortical venous varixventricular drainage, resection of nidus, excision of venous varix, no residualasymptomatic, 36 mos
1070, Msubarachnoid & ventricular hemorrhagetentorial incisuralt tentorial & ECA branches, low flowgalenic, prepontine variceal venous drainagesurgical excision, no residualasymptomatic, 24 mos

AVM = arteriovenous malformation; ICA = internal carotid artery; ECA = external carotid artery; PCA = posterior communicating artery; SCA = superior cerebellar artery.

Retrograde leptomeningeal venous drainage was identified in all 10 aggressive cases, and was variceal or aneurysmal in nine. This appeared to be the source of bleeding in every hemorrhagic case. Six patients had high angiographic flow, strickly defined as the appearance of the dural AVM venous phase prior to filling of the distal territory of major feeding arteries.

Two patients died from cerebral hemorrhage. In one this was possibly related to low-dose anticoagulation therapy for pulmonary embolism. A third patient was severely disabled by catastrophic cerebral hemorrhage sustained after a temporal lobe meningeal biopsy which had been performed to rule out a chronic leptomeningeal process in the setting of atypical rostral brain-stem dysfunction and abnormal cerebrospinal fluid analysis. Six patients underwent surgical excision of the dural AVM nidus and disconnection of leptomeningeal draining veins; in two of these, preparatory, staged embolizations were performed preoperatively. One patient underwent embolization and radiation therapy for an extensive nonresectable nidus diffusely involving the floor of the middle fossa. The seven treated patients are doing well after a mean follow-up period of 30 months, despite residual nidus in two cases. Illustrative radiological studies of Cases 2, 6, and 8 are presented in Figs. 1, 2, and 3.

Fig. 1.
Fig. 1.

Case 2. Tentorial and transverse sinus dural arteriovenous malformation and acute cerebellar and ventricular hemorrhage. Upper: Computerized tomography scans. Lower: Right common carotid arteriogram, anteroposterior view. Arterial feeders include the occipital arteries and tentorial branches of the internal carotid arteries. Drainage is via the transverse sinus and multiple retrograde variceal leptomeningeal veins including a giant venous aneurysm. The patient died despite supportive measures.

Fig. 2.
Fig. 2.

Case 6. Tentorial incisural dural arteriovenous malformation (AVM) and acute thalamic and ventricular hemorrhage. A: Computerized tomography scan revealing hemorrhage into the pulvinar of the right thalamus and intraventricular spillage. B: Right internal carotid arteriogram, lateral view, revealing a premature venous blush at the torcular and a venous aneurysm at the tentorial incisura. C: Same injection, anteroposterior view, during the early venous phase revealing the aneurysm and the galenic venous system and transverse sinus. D: Selective external carotid arteriogram, lateral view, visualizing the same venous aneurysm filling via middle meningeal branches. The aneurysm presents a small daughter sac superiorly, which was the site of hemorrhage. The tentorial leaflet and enclosed dural AVM nidus were resected via a right subtemporal approach.

Fig. 3.
Fig. 3.

Case 8. Right transverse sinus dural arteriovenous malformation (AVM) and acute temporal lobe hemorrhage. A: Computerized tomography (CT) scan showing intracerebral hematoma. B: Contrast-enhanced CT scan showing serpentine enhancement of vascular channels above and below the tentorial incisura. C: Right external carotid arteriogram, oblique view, showing high-flow shunting into the ipsilateral sigmoid-jugular system. D: Right external carotid arteriogram, lateral view, after embolization of several feeders; the site of shunting of the dural AVM nidus is now clearly localized to the middle third of the right transverse sinus. After multiple embolizations, the right transverse sinus and adjacent dura and tentorium were resected en bloc. E: Postoperative panangiography revealed no residual AVM (right external carotid injection shown).

Nonaggressive Cases

Table 2 summarizes the clinical and angiographic features of the seven patients without an aggressive neurological course. There were five women and two men with a mean age of 61.6 years (range 29 to 75 years). Four patients presented with pulsatile tinnitus, two of whom had suffered head trauma many years before (possibly incidental or unrelated). On physical examination, two patients were found to have cervical bruit and underwent angiography for that reason, thereby revealing the dural AVM. One patient presented with pain and partial ophthalmoplegia. Mean duration of symptoms in the symptomatic cases was 1 year (range 3 months to 2 years).

TABLE 2

Clinical and angiographic features of seven patients with nonaggressive dural AVM's*

Case No.Age (yrs), SexHistoryClinical PresentationDural AVM LocationArterial SupplyVenous DrainageTreatmentOutcome & Follow-Up Period
1166, Ftrauma in childhood, pulsatile tinnitus & bruit for 1 yrsamelt transverse sinuslt ECA & tentorial branches, high flowtransverse sinus, no cortical drainage or varicestinnitus less noticeable, 18 mos
1229, Ftrauma at age 9, headache, pulsatile tinnitus for 2 yrssame, orbital & cranial bruitrt cavernous regionrt ICA & ECA, low flowcavernous sinusno change in symptoms, 14 mos
1369, Frt mastoid bruitrt transverse sigmoid sinusrt tentorial branches of ICA, bilat occipital & vertebral arteries, high flowtransverse sinus, no cortical drainage or varicesasymptomatic, 12 mos
1475, Mcervical bruitlt transverse sigmoid sinusbilat occipital & vertebral arteriestransverse sinus, no cortical drainage or varicesasymptomatic, 18 mos
1568, Mpulsatile tinnitus for 1 yrsamelt transverse sigmoid sinuslt ECA & tentorial branches, low flowtransverse sinus partially occluded, retrograde pial drainage to cerebellum & cerebrum, varicealtinnitus less noticeable, 14 mos
1652, Fpulsatile tinnitus for 8 mossamelt transverse sinuslt ECA & tentorial branchessigmoid sinus thrombosis, drainage via contralateral transverse sinus, no cortical drainage or varicesno change in symptoms, 19 mos
1772, Fpartial ophthalmoplegia, facial pain for 3 mossamelt cavernous regionleft ECA & bilat ICA branchescavernous sinusembolization, no residual shuntinitial improvement, transient “paradoxical” worsening of eye symptoms 3 mos postembolization, angiograms negative

AVM = arteriovenous malformation; ECA = external carotid artery; ICA = internal carotid artery.

The dural AVM was located at the transverse sinus in five cases and at the cavernous sinus in two. There was leptomeningeal venous drainage in only one case, and it was variceal. None of the AVM's had galenic venous drainage. Five of the seven lesions had high angiographic flow.

Six of these nonaggressive AVM's were managed conservatively. In Case 17, the lesion was successfully embolized with transient improvement of facial pain and eye symptoms; however, 3 months later, ophthalmoplegia partially recurred. A repeat angiogram did not reveal residual or recurrent dural AVM, and the clinical deterioration was consistent with the “syndrome of paradoxical worsening” secondary to ophthalmic vein thrombosis.92 This patient's symptoms have gradually resolved spontaneously. The follow-up period for these nonaggressive cases has been short (mean 16 months, range 12 to 19 months).

Literature Meta-Analysis

We retrieved the reports of 360 dural AVM's which appeared in the literature prior to March, 1989, and which contained sufficient clinical and angiographic information for meaningful analysis.1–114 Thus, including our 17 cases, 377 dural AVM's were included in this analysis. One hundred cases exhibited an aggressive neurological course as defined (88 cases with hemorrhage and 12 cases with nonhemorrhagic focal neurological deficit other than ophthalmoplegia). The other 277 AVM's did not exhibit an aggressive neurological course as defined (203 patients presented with pulsatile tinnitus, 39 with ophthalmoplegia, and 10 with papilledema and/or postpapilledema optic atrophy; the remaining patients were asymptomatic or had head or facial pain).

Table 3 summarizes the AVM location in relation to aggressive neurological behavior. Dural AVM's at the tentorial incisura accounted for 8.4% of reported cases and were most often associated with aggressive neurological behavior. Dural AVM's at the transverse-sigmoid sinuses and at the cavernous sinus accounted for 62.6% and 11.9% of reported cases, respectively, and were least likely to be associated with aggressive neurological behavior. No location of dural AVM's was immune from aggressive neurological behavior.

TABLE 3

Relationship of dural AVM location to aggressive neurological behavior*

Location of AVMCasesAggressive Cases (A)Non-aggressive Cases (B)Ratio A:B
No.%    
orbital-falx-anterior fossa225.81572.1:1
convexity-sagittal sinus287.414141:1
sylvian-middle fossa143.71042.5:1
cavernous sinus4511.96391:6.5
tentorial incisura328.431131:1
transverse-sigmoid sinuses23662.6242121:8.8
total cases377100277

AVM = arteriovenous malformation.

Percent of the total 377 cases.

Table 4 summarizes particular angiographic features of dural AVM's in relation to aggressive neurological course. Leptomeningeal retrograde venous drainage, variceal or aneurysmal venous dilations, and galenic venous drainage each correlated significantly with aggressive neurological course as defined. These angiographic features frequently coexisted in the same case, and none emerged as a truly independent risk factor in multivariable analysis. Every dural AVM with an aggressive neurological course exhibited one or more of these three features, while less than 1% of the nonaggressive AVM's exhibited them simultaneously. Contralateral arterial contribution and the presence of high-flow shunting (defined as the appearance of a dural AVM venous phase prior to filling of the distal territory of major feeding arteries) were not associated with aggressive neurological behavior.

TABLE 4

Association of angiographic features with aggressive neurological behavior*

FactorLeptomeningeal Retrograde Venous DrainageVariceal or Aneurysmal Venous StructuresGalenic Venous DrainageHigh-Flow ShuntingContralat Arterial Contribution
yesnoyesnoyesnoyesnoyesno 
aggressive lesion8084635205327294137
nonaggressive lesion4223920206326343242930
significancep < 0.001p < 0.001p < 0.05NSNS

Information regarding these angiographic features was not available in every case. High-flow shunting and aggressive and nonaggressive neurological behavior are strictly defined in the text. NS = not significant.

Significance: exact chi-square or Fisher's exact p value.

The 12 cases with nonhemorrhagic focal neurological deficit had some common features peculiar to them. In all 12 cases, the dural AVM involved the tentorial incisura with medial drainage into the galenic system or prepontine veins via venous varicosities or aneurysms. In one case, there was autopsy verification of diencephalic necrosis attributed to venous hypertension.71 Despite these common features, we could not identify specific sufficient criteria unique to this small group of cases. Another 19 cases of tentorial dural AVM's with medial or galenic drainage did not exhibit nonhemorrhagic brain-stem dysfunction.

The 10 cases with papilledema, arbitrarily considered in this study with nonaggressive lesions, had common features. All involved superior sagittal, torcular, or transverse sinus locations, with high flow, bilateral arterial contribution, and venous outflow stenosis. While these features were present in every patient with papilledema, other lesions with similar features did not manifest this problem. The incidence of venous outflow obstruction among cases without papilledema could not be estimated since the presence or absence of venous outflow obstruction is rarely noted in published reports.

Discussion

Much has been learned in recent years about dural AVM's. It has been well established that the majority of these lesions are acquired.38,97 There is also uniform agreement that individual symptomatology is dependent on lesion location,16,34,35,51,54,56,58,72,79,111 and that focal neurological complications are related to patterns of venous drainage.17,19,25,35,37,56,58,63,71,82,111 The natural history of these lesions is highly variable. Spontaneous thrombosis and/or regression are not uncommon.7,33,61,81 Some lesions may exhibit benign symptomatology for many years;3,8,16,20,79 however, a fraction of dural AVM's manifest more aggressive behavior including cerebral hemorrhage and progressive nonhemorrhagic neurological deficit.17,19,21,24,35,41,56,63,111 It is not clear which features represent necessary and sufficient criteria to cause this behavior.

Factors Predisposing to an Aggressive Neurological Course

Our experience with 17 dural AVM's, including 10 lesions with aggressive neurological behavior, suggests the presence of common features in aggressive cases; however, the small number of patients in this and in all other reported series makes statistical conclusions difficult. It is not known if and to what extent these common features of aggressive lesions might also be present in nonaggressive cases. In the absence of conclusive prospective studies, a multitude of retrospective reviews have attempted to tackle these questions. Several reviews have concentrated on individual types of dural AVM or on a particular symptomatology. By not examining other dural AVM's, they could not reach firm conclusions regarding natural history nor could they shed inherent selection bias imposed by their scope. Nevertheless, these reports have served to elucidate the pathophysiology of certain symptoms16,22,45,69,72,79,92 or to underline therapeutic approaches to specific lesions.26,27,29,39,42,43,65,75,78,79,97,111 In other instances, they have provided evidence of acquired etiology,8,38,70,86,113 and of lesion progression.2,17,35,63,71,111

More comprehensive reviews of the literature have recently been compiled by Malik, et al.,63 and Lasjaunias, et al.56 The study by Malik, et al., published in 1984, examined 223 dural AVM cases reported prior to 1983, including the authors' six cases with hemorrhage and four cases without hemorrhage. Malik, et al., advanced the hypothesis that lesions related to large dural sinuses are less likely to bleed than lesions with “restricted dural venous outflow” such as galenic lesions. They did not compare statistically other features of lesions with and without hemorrhage, and did not perform a detailed analysis by lesion location other than proximity to a major sinus. The absence of these correlations invited two critical responses, one by Lasjaunias, et al.,58 suggesting factors other than AVM location, and one by Parkinson83 essentially questioning whether dural AVM's adjacent to major sinuses can ever bleed.83

The analysis of the literature presented by Lasjaunias, et al.,56 in 1986 contributed four new cases and reviewed another 191 cases selected from the literature. The criteria for selection of these 191 cases from over 250 dural AVM's published to that date were not given. A statistical analysis of features of hemorrhagic and nonhemorrhagic cases was not presented. Instead, the authors presented a scholarly (although qualitative) analysis of lesion location and angiographic features in relation to individual symptoms including hemorrhage. They synthesized the thoughts of most authors to date by suggesting that lesion location essentially determines the type of symptom, and that drainage characteristics are responsible for focal neurological complications. The incidence of individual features among lesions with or without aggressive neurological behavior was not presented.

Since these reviews, other aggressive dural AVM's have been reported,24,26–30,41,66,71,104,111 and the authors have generally concurred with the thesis of Lasjaunias, et al.56 We chose to perform an updated review of all published dural AVM cases with sufficient clinical and angiographic information.1–114 The objective of the review was to statistically correlate lesion location and various angiographic features with aggressive neurological behavior, in order to confirm or question the previously advanced hypotheses. We reviewed a total of 377 dural AVM's: the 17 cases reported here; 122 cases reported between January, 1984, and March, 1989; 209 of the cases reviewed by Malik, et al.;63 and 29 dural AVM's reported prior to 1984 but not referenced by Malik, et al.

Lesion Location

Among these reported cases, no lesion location was immune from aggressive neurological behavior. A dural AVM location at the tentorial incisura was most ominous, with 31 of 32 cases associated with hemorrhagic or nonhemorrhagic stroke. Lesions at the cavernous sinus and at the transverse-sigmoid sinuses appeared least associated with aggressive neurological behavior. Yet even in these locations, more than one of the 10 reported lesions behaved aggressively.

We acknowledge an inherent selection bias toward aggressive lesions in case reports, and cannot be certain from this information if location alone dictates the higher risk. It could well be that the location of the lesion might disclose some cases in view of the particular clinical symptomatology, such as pulsatile tinnitus and ophthalmoplegia, while lesions in other locations might not exhibit any symptoms until they behave aggressively. This would be consistent with the thesis proposed by Malik, et al.,63 but would not exclude other risk factors as suggested by Lasjaunias, et al.56,58

Angiographic Features

Detailed analysis of angiographic features of reported dural AVM's further clarifies these issues. Leptomeningeal retrograde venous drainage, variceal or aneurysmal venous structures, and galenic venous drainage were significantly associated with aggressive clinical behavior. Not a single case with an aggressive neurological course has been reported without at least one of these features. However, a small proportion of nonaggressive lesions also exhibited one or more of these features. The precise risk of future hemorrhage from such lesions cannot be estimated. Nevertheless, several reports clearly documented progression toward aggressive behavior after intervals of months to years.2,17,35,63,71,111 The first hint of aggressive behavior is commonly associated with very high morbidity. Available information strongly suggests a several-fold increased risk of aggressive behavior in the presence of these features. This warrants, in our opinion, an aggressive clinical stance toward lesions with these features, which would include vigilant follow-up monitoring or prophylactic therapeutic intervention, depending on the individual case.

The presence of contralateral arterial contribution or high-flow shunting did not correlate with aggressive neurological behavior. These features undoubtedly affect the complexity and/or morbidity of therapeutic interventions and the severity of “neighborhood symptoms” such as pulsatile tinnitus, pain, and ophthalmoplegia. In the presence of venous outflow obstruction, they might also contribute to the risk of papilledema. Therefore, these features do affect therapeutic strategy, even if they do not strictly imply increased risk of hemorrhage. Our review helps clarify the syndrome of nonhemorrhagic brain-stem dysfunction from dural AVM's. The 12 reported cases (including two of our own) all involve tentorial lesions with prepontine or galenic variceal venous drainage. The one autopsied case revealed venous congestion and parenchymal necrosis consistent with a pathophysiology of venous hypertension.71 We suspect that segmental venous hypertension results in decreased focal perfusion pressure as well as venous congestion.

Natural History

In conclusion, our experience with dural AVM's and a review of the relevant literature suggest the presence of several stages in the natural history of these lesions (Fig. 4). Microscopic communications between arteries and veins exist in normal dura mater at the proximity of venous sinuses.47,108 Trauma, surgery, sinus thrombosis, or other factors might initiate the genesis of a true dural AVM.57,59,86 Subsequent progression from one stage to the next has been documented.8,38,70,86,113 The clinical behavior of dural AVM's, including initial presentation, eventual behavior, and prognosis, is a complex function of multiple and interrelating factors such as lesion location, patterns of arterial supply, and venous drainage (Fig. 5). Host-related angiological or hematological mechanisms, including hormonal and hemostatic factors, might also play a role. Each of these factors affects therapeutic strategies as well; however, venous drainage remains the primary determinant of catastrophic neurological behavior.

Fig. 4.
Fig. 4.

Artist's illustration of three possible stages in the natural history of a dural arteriovenous malformation (AVM). A: Sinus thrombosis and engorged dural venous collaterals with opening of embryonic arteriovenous communications. B: Arteriovenous shunting favors recruitment of arterial feeders into the nidus (sump effect) with secondary venous hypertension. C: Venous hypertension favors leptomeningeal retrograde venous drainage and predisposes such channels to become varicose and aneurysmal. These three stages can be clearly documented in dural AVM's from our experience and from the literature.

Fig. 5.
Fig. 5.

Diagram of various stages of evolution in the natural history of dural arteriovenous malformations (AVM's) and of pathophysiological consequences and clinical manifestations of each stage. * = Probably accentuated by venous outflow obstruction; † = possibly triggered by extension of sinus thrombosis; ‡ = symptoms due to flow or local arterial or venous congestion.

The therapeutic armamentarium includes conservative monitoring,3,7,20,33,81 arterial embolization (with balloons, particles, or chemicals),19,28,36,46,64,87,98,109,111 transvenous occlusion,26,27,29,99,103,114 surgical excision,39,63,97,111 and radiation therapy. One or more of these options might represent the best strategy for an individual case after thorough analysis of all angiographic and pathophysiological features of the lesion and its past and potential clinical behavior. In general, endarterial techniques decrease or eliminate the arteriovenous shunt, but rarely succeed in obliterating all arterial feeders or the fistula itself. Transvenous techniques are designed to thrombose the sinus segment adjacent to the dural AVM, with the objective of propagating thrombosis into the AVM itself. Surgical therapy, with or without preparatory embolization, remains the most versatile and effective therapeutic option. It is usually aimed at resecting the dural leaflets harboring the AVM (and adjacent sinus) and at disconnecting leptomeningeal draining pathways which are typically the source of serious neurological sequelae.

Acknowledgments

We acknowledge the contribution of Robert Spetzler, M.D., and L. Phillip Carter, M.D., to the management of Cases 2 and 7; Stanley Shatsky, M.D., and Ira Fink, M.D., to the management of Case 8; and Sylvain Palmer, M.D., Anthony Stoffer, M.D., and Michael Pritz, M.D., Ph.D., to the management of Case 6. Statistical analysis was performed with the assistance of Chris Skibinski, M.S., of the Department of Biostatistics and Epidemiology of the Cleveland Clinic Foundation. The drawings were carried out by Mr. Joe Kanasz of the Art Department of the Cleveland Clinic Foundation. The manuscript was expertly prepared by Ms. Shirley McDaniel.

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This paper was presented at the Annual Meeting of the American Association of Neurological Surgeons, Washington, D.C., April 1–6, 1989.

Article Information

Address reprint requests to: Issam A. Awad, M.D., Department of Neurological Surgery, S80, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, Ohio 44195–5275.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Case 2. Tentorial and transverse sinus dural arteriovenous malformation and acute cerebellar and ventricular hemorrhage. Upper: Computerized tomography scans. Lower: Right common carotid arteriogram, anteroposterior view. Arterial feeders include the occipital arteries and tentorial branches of the internal carotid arteries. Drainage is via the transverse sinus and multiple retrograde variceal leptomeningeal veins including a giant venous aneurysm. The patient died despite supportive measures.

  • View in gallery

    Case 6. Tentorial incisural dural arteriovenous malformation (AVM) and acute thalamic and ventricular hemorrhage. A: Computerized tomography scan revealing hemorrhage into the pulvinar of the right thalamus and intraventricular spillage. B: Right internal carotid arteriogram, lateral view, revealing a premature venous blush at the torcular and a venous aneurysm at the tentorial incisura. C: Same injection, anteroposterior view, during the early venous phase revealing the aneurysm and the galenic venous system and transverse sinus. D: Selective external carotid arteriogram, lateral view, visualizing the same venous aneurysm filling via middle meningeal branches. The aneurysm presents a small daughter sac superiorly, which was the site of hemorrhage. The tentorial leaflet and enclosed dural AVM nidus were resected via a right subtemporal approach.

  • View in gallery

    Case 8. Right transverse sinus dural arteriovenous malformation (AVM) and acute temporal lobe hemorrhage. A: Computerized tomography (CT) scan showing intracerebral hematoma. B: Contrast-enhanced CT scan showing serpentine enhancement of vascular channels above and below the tentorial incisura. C: Right external carotid arteriogram, oblique view, showing high-flow shunting into the ipsilateral sigmoid-jugular system. D: Right external carotid arteriogram, lateral view, after embolization of several feeders; the site of shunting of the dural AVM nidus is now clearly localized to the middle third of the right transverse sinus. After multiple embolizations, the right transverse sinus and adjacent dura and tentorium were resected en bloc. E: Postoperative panangiography revealed no residual AVM (right external carotid injection shown).

  • View in gallery

    Artist's illustration of three possible stages in the natural history of a dural arteriovenous malformation (AVM). A: Sinus thrombosis and engorged dural venous collaterals with opening of embryonic arteriovenous communications. B: Arteriovenous shunting favors recruitment of arterial feeders into the nidus (sump effect) with secondary venous hypertension. C: Venous hypertension favors leptomeningeal retrograde venous drainage and predisposes such channels to become varicose and aneurysmal. These three stages can be clearly documented in dural AVM's from our experience and from the literature.

  • View in gallery

    Diagram of various stages of evolution in the natural history of dural arteriovenous malformations (AVM's) and of pathophysiological consequences and clinical manifestations of each stage. * = Probably accentuated by venous outflow obstruction; † = possibly triggered by extension of sinus thrombosis; ‡ = symptoms due to flow or local arterial or venous congestion.

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