Morphologic Change of Flow-Related Aneurysms in Brain Arteriovenous Malformations after Stereotactic Radiosurgery

Discussion

The exact mechanism of FA formation in BAVMs is not fully understood. Increased blood flow stress of the BAVM is presumed to be a major factor undoing the balance between hemodynamic stress and the integrity of the internal elastic lamina and intima of the arterial wall. Rapid or turbulent blood flow in the feeders of BAVMs is also reported to be a more important hemodynamic factor in FA formation than intravascular pressure.² Previous studies had shown that older patients with larger BAVMs and posterior circulation supply to the BAVM are prone to FAs.^9,10 The reported incidence of FAs ranges from 6% to 27%.^{4,9,10⇓⇓⇓⇓⇓–16} This variation of the incidence of FAs may be attributed to different criteria of FA and DSA protocols, overlooked small FAs, and a lack of superselective microcatheterization of cerebral arteries.¹⁷ In the past, conventional 2D-DSA was the criterion standard method of evaluating BAVM angioarchitecture. Nevertheless, because of the overlap of FAs by the parent artery or arterial branch on conventional DSA and the lack of rotational and 3D-reconstruction DSA, 2D-DSA may overlook 6.8%–21% of intracranial aneurysms, particularly, aneurysms of <3 mm.^{18⇓⇓–21}

In our series, the incidence of FAs was 8.8%; this was within the range of previously reported rates but slightly lower than the average detection rate. The lower detection rate was likely due to the lack of superselective microcatheter DSA in all patients and the absence of rotational/reconstruction DSA in 42% of patients in our series. Multiple FAs were found in 26 of 72 patients (36%); the number of FAs per patient was 1.5. The frequency of multiple FAs in our series was compatible with that in the series of Redekop et al,² in which 123 FAs occurred in 71 patients, but it was much higher than that in the series of Morgan et al⁹ with 4 of 67 patients (6%) with multiple FAs. Most FAs are small and <8 mm.^4,8,9,22 In our series, all FAs were small (mean size, 4.1 mm), with proximal FAs (mean size, 4.3 mm) being a little larger than distal FAs (mean size, 3.7 mm). However, in recently published data of 172 hemodynamic saccular aneurysms of BAVMs,⁸ 62% of aneurysms were <6 mm, but 38% of aneurysms were >7 mm, with 17% of aneurysms >16 mm. This result may be attributed to the coincidence of natural intracranial aneurysms with BAVMs.

The annual growth rate of most natural unruptured intracranial aneurysms is highly variable and unpredictable.¹⁵ Spontaneous partial or complete thrombosis is uncommon in intracranial aneurysms.²³ FAs can be differentiated from natural unruptured intracranial aneurysms because they are impacted by the hemodynamic stress of BAVMs, and the latter are not. In our series, FAs tended to be regressive in larger BAVMs (P = .048) and smaller FAs (P = .0001) during follow-up and showed statistical significance, but there was no statistical significance in sex (P = .70), patient age (P = .21), ruptured/unruptured BAVMs (P = .85), or complete/incomplete obliteration of BAVMs (P = .29). Larger BAVM obliteration was usually associated with greater alteration of hemodynamics, leading to size regression of FAs. Smaller FAs were more commonly found in distal FAs than proximal FAs. Redekop et al² reported the tendency of distal FAs to spontaneously disappear after complete BAVM occlusion, which occurred in 4 of 5 FAs (80%) in their series, whereas only 21.7% (23 of 106 proximal FAs) decreased in size after BAVM treatment. This result was similar to our results with statistical significance (P < .001): Thirty-three of 40 (83%) distal FAs partially or totally disappeared, but only 18 of 71 (25%) proximal FAs regressed in size or totally disappeared. In terms of the individual territory of size regression of distal-versus-proximal FAs, the MCA territory showed statistical significance (P = .01), but the territories of the ACA and infratentorium were not statistically significant (P = .19, P = .052).

Spontaneous thrombosis of a distal FA tends to occur largely because most distal feeders provide blood to the BAVM, where total BAVM obliteration usually leads to total occlusion and significant reduction of the caliber of the distal feeder and thereby to total or partial regression of the FA. By contrast, the parent artery of proximal FAs supplies both normal brain tissue and the BAVM, where total or subtotal occlusion of the BAVM normalizes the blood flow of the parent artery, reducing the hemodynamic stress on feeders; however, the hemodynamic flow from the normal parent artery to the proximal FA persists, reducing the frequency of spontaneous thrombosis of proximal FAs to less than that of distal FAs. Although small-sized FAs tended to disappear after integration of the data of all territories (P = .04), the frequency of FA regression was not statistically significantly related to FA size in individual territories of the MCA (P = .36), ICA (P = .57), and infratentorium (P = .31). In our study, there was no significant enlargement of FA size at a mean 58-month DSA follow-up.

Stereotactic radiosurgery has been widely used to manage patients with BAVMs with promising results. The reported cure rate for BAVMs at 3 years after stereotactic radiosurgery may be as high as 56%–85% in some selected patients.^6,24 In terms of peritherapeutic hemodynamic change, GKS differs from endovascular embolization and surgical removal by obliterating BAVMs gradually and slowly so that the hemodynamic impact on brain tissue and FAs is progressively decreased with less risk of an acute sudden increase in the transmural pressure across the dome of the FA, leading to rupture. Previous studies had shown that the presence of an associated aneurysm significantly increases the risk of rehemorrhaging after stereotactic radiosurgery.⁶ FAs are an independent determinant for increased risk of incident BAVM hemorrhage²¹, and FAs may change the natural course of BAVM with increasing hemorrhage.⁹ These findings suggest the need for additional interventional management of the aneurysm to reduce the risk of bleeding during the latency interval after stereotactic radiosurgery for BAVMs.^6,7 However, in our 72 patients with 111 FAs and an average of 58 months of angiographic and clinical follow-up, only 2 patients developed a ruptured FA; 1 rupture had fatal consequences. The rupture rate per aneurysm/year was calculated to be 0.37%, and the incidence of FA rupture was similar to that reported for natural unruptured intradural aneurysms.^25,26

Aggressive management of FAs has been reported with promising results.⁸ For distal FAs that usually have a wide neck or fusiform dilation, it is feasible in some selected patients to perform embolization with liquid embolic materials to obliterate the BAVMs and distal FAs in the same session.⁴ For small smooth-contoured proximal FAs with a relatively low risk of rupture, conservative management is an acceptable option. Nevertheless, with ruptured or symptomatic FAs, proximal FAs larger than 5 mm, irregularly shaped FAs, and those patients with a family history of a ruptured aneurysm, aggressive management by interventional procedures is indicated. Because most proximal FAs are wide-necked, stent-assisted coiling may be necessary to prevent coil migration to the parent artery; however, this technique should be used with caution because of the need for peritherapeutic antiplatelet medication to prevent stent-related thromboembolic complications. Antiplatelet treatment will worsen bleeding from ruptured or reruptured BAVMs or residual BAVMs. The technique of balloon-assisted FA coiling is an alternative. It is better to perform stent-assisted coil embolization and endovascular management of BAVMs during the same session to totally eliminate the risk of bleeding or rebleeding (eg, bleeding from an intranidal aneurysm) rather than wait for total obliteration of the BAVM. In our series, most FAs were small (mean size, 4.1 mm). Considering the natural course of small, unruptured FAs, most of our FAs were conservatively managed by neuroimaging follow-up.

There were some limitations to our study: First, this is a retrospective study of long duration. A prospective study is warranted to confirm our observations, and the mean angiographic follow-up time is not long enough to justify the real morphologic change of FAs after GKS. Second, some patients did not undergo rotational DSA, and all patients lacked microcatheter angiography. These factors may lead to underestimating the true incidence of FAs, particularly distal FAs, because of superimposition on BAVMs.