Intracranial dural arteriovenous fistula and arteriovenous malformation discovered incidentally after stroke

Dear Editor,

Intracranial vascular malformations with arteriovenous shunt are rare conditions, including both acquired and congenital diseases. The main representative of the acquired category is the dural arteriovenous fistula (DAVF). Conversely, arteriovenous malformations (AVMs) are considered congenital lesions. Both malformations can be incidentally found, but usually, they are searched in case of hemorrhagic stroke. The hemorrhagic risk related to each type of malformation (DAVF and AVM) is defined on the basis of angioarchitecture and usually requires catheter angiography.[1,2]

On the other hand, ischemic stroke is a common cerebrovascular event, and it is treatable using intravenous thrombolysis (IVT) and, when a large vessel occlusion (LVO) is identified, endovascular thrombectomy (EVT). The coexistence of several cerebrovascular diseases in the same patients is not a common occurrence.

Case Presentation

A 56-year-old male went to our attention because of the occurrence of left-sided hemiplegia and dysarthria at awakening. His past medical history was significant for several vascular risk factors (arterial hypertension, diabetes, dyslipidemia, and past smoking) and previous vascular events (acute coronary syndrome leading to bypass and peripheral arteriopathy). NIHSS score was 14, and last time to seen well (LTSW) was 5 h at hospital admission. Noncontrast computed tomography (NCCT) did not show any hyperacute change in brain parenchyma. CT angiography (CTA) found a tandem steno-occlusion involving the right intracranial internal carotid artery (ICA) and M1 middle cerebral artery (MCA) and, as incidental finding, the early contrast opacification of a superficial venous channel in the right occipital location [Figure 1a]. The CT perfusion pattern showed a wide hypoperfused volume in the right MCA territory with a pattern supporting the penumbra hypothesis. The patient underwent IVT and was referred for endovascular treatment. The first angiographic series documented the recanalization of the right ICA and a partial restoration of flow in the right M1 MCA with a residual irregular stenosis, suggestive for a fixed focal stenosis [Figure 1b]. A dural arteriovenous shunt was documented in the right occipital location, with an arterial supply from several external carotid artery (ECA) branches, supporting the CTA hypothesis of DAVF. The acute stroke setting prevented a complete evaluation of this component. The patient underwent a quick neurological improvement after starting IVT, and the NIHSS score was 0 at 24 h. The final lesion balance was highly positive on magnetic resonance imaging (MRI) [Figure 1c-e]. Dual antiplatelet therapy was started 24 h after IVT, and an aggressive secondary prevention strategy was performed.

Figure 1.

(a) Baseline intracranial computed tomography angiography (axial plan, maximum intensity projection/multiplanar reconstruction [MIP/MPR]), showing the right internal carotid artery (ICA) terminus, A1 anterior cerebral artery and M1 middle cerebral artery (MCA) steno-occlusion. As an incidental finding, a superficial venous channel in the right occipital lobe was opacified in the arterial phase. (b) Digital subtraction angiography (DSA) in PA view from right ICA injection with patent ICA and M1 MCA with an irregular CA stenosis. Brain magnetic resonance imaging 5 days after stroke, showing a very small periventricular lesion, hyperintense in FLAIR (c) and diffusion-weighted imaging (d) and hypointense in apparent diffusion coefficient (ADC) map (e). Follow-up DSA with a detail on right M1 MCA stenosis in PA view from seriogram (f), 3D-RA with virtual reality (g), and MIP/MPR (h)

After the successful management of the acute stroke, the incidental findings were addressed. Then, a diagnostic digital subtraction angiography (DSA) was planned, aiming to better evaluate the angioarchitecture and hemodynamics of the DAVF and, at the same time, assess the evolution of the right MCA stenosis. About this last issue, DSA confirmed the right MCA recanalization, which is characterized in its proximal M1 segment by moderate stenosis (51% according to WASID protocol). In addition, the opacification of the vessels of the Sylvian group on the right side appeared regular with normal capillary and venular filling times, excluding a hemodynamic role for the stenosis. In addition, the main lenticulostriate arteries arise close to the stenosis [Figure 1f-h]. Moving to the DAVF characterization, the study of the right ECA confirmed the DAVF fed by the posterior branch of the middle meningeal artery (MMA) and by the transosseous branch of the right occipital artery (OA) with direct venous drainage into the occipitopolar cortical vein. This last one is characterized by slight tortuosity and initial increase in diameter and with subsequent course toward the mesial venous compartment [Figure 2a-d]. The selective catheterization of the right vertebral artery (VA) highlights ostial stenosis, but the injection of the left VA provided a further incidental finding, i.e., an arteriovenous shunt with a nidus fed by left anterior–inferior cerebellar artery (AICA) branches and draining into a left middle cerebellar vein. It was a small pial AVM located at the surface of the left middle cerebellar peduncle [Figure 2e-h].

Figure 2.

Follow-up digital subtraction angiography (DSA) with a complete definition of the arterial supply of the dural arteriovenous fistula from right external carotid artery injection, showing as supplying branches the petro-squamous branch of the middle meningeal artery (with two separated peduncles) and OA (transosseous branches) (a and b in lateral view) with details in c and d and evidence of an ectatic, tortuous occipitopolar vein as drainage route. DSA from left VA injection in PA (e and f) and lateral (g and h) views, showing the left-sided nidus fed by AICA branches and drained by the left middle cerebellar vein. (f and h) are 3D-RA with MIP/MPR

The DAVF was evaluated as Cognard type Iia,[1] and an endovascular treatment was proposed and successfully performed under general anesthesia [details in the caption of Figure 3]. Posttreatment, NCCT did not show unwanted complications, and the patient was neurologically normal.

Figure 3.

The patient underwent endovascular embolization by means of superselective injection with microcatheterization of nonadhesive embolizing liquid (SQUID 18), though a carrier catheter (Neuron MAX®088) in right common carotid artery and a coaxial catheterization [AXS Catalyst 5 distal access catheter (Stryker Neurovascular)], whose distal end is placed in the first segment of the right internal maxillary artery near the origin of the middle meningeal artery (MMA). A microcatheterization of the MMA (DMSO compatible microcatheter: Sonic 1.2-F microcatheter [BALT Extrusion, Montmorency, France]) allowed to gain the petrosquamous branch and navigate into the vessel, reaching a position close to the point of fistula. Then, a multiphase injection of nonadhesive embolizing liquid (Squid 18: 0.7 mL) was performed with good progression of the material and exclusion of the venous components and in particular of the proximal ectatic venous portion of the dural arteriovenous fistula (DAVF). At the final angiographic control, the exclusion from the circulation is confirmed with preservation of the arteriolar–capillary phases and venous drainage time (in particular in the right temporo-occipital region). In particular, post-treatment DSA demonstrated the occlusion of DAVF (a, lateral view from right external carotid artery injection) and the corresponding cast of SQUID 18 in b

Discussion

The presented case has a series of peculiarities, starting from the acute stroke and continuing to two relevant incidental findings, i.e., asymptomatic DAVF and AVM. The main feature is that these three cerebrovascular conditions are independent each from the other one and not causally related. However, all these conditions are potentially relevant to the patient’s prognosis and affect the treatment. The patient came to the attention of the neurologist in emergency for an acute ischemic stroke with an occlusive pattern from LVO represented by a tandem occlusion of intracranial ICA and MCA M1 on a systemic atherothrombotic background. Even in this prognostically unfavorable context, IVT determined a complete recanalization with minimal final ischemic lesion, revealing an underlying stenosis of the right MCA M1, which, however, can hardly be attributed as a cause of the occlusive pattern indicated above, regardless of the very favorable response to IVT alone. Furthermore, the previous coronary artery disease determined a cardiac wall hypokinesia with antecedent of apical thrombosis of the left ventricle. In the current stroke, the echocardiographic study, carried out postfibrinolysis, did not reveal any intracavitary thrombotic formations. As a further element, the brain MRI did not show any old infarctions in the MCA territory or signs of hemodynamic insufficiency conditioned by the stenosis of the M1 MCA, which, however, angiographically presented a normal arteriocapillary filling time compared to the contralateral district. All the above considerations led to the choice to continue maximal medical therapy, in accordance with the guidelines.[3]

Neuroradiological investigations performed during the management of the acute stroke highlighted two different incidental findings in sequence, whose coexistence in the same subject is extremely rare, namely a DAVF and a pial AVM, which were not correlated with each other in any way.

Intracranial vascular malformations are rare diseases, with a detection rate of 0.15–0.29/100,000/year and 1.12/100,000/year for DAVF and AVM, respectively.[4,5] The first reference[4] is a Scottish population study evaluating two years (1999 and 2000) with several sources of information and a retrospective revision of the imaging and autopsy, when possible (95% of cases). Using this approach, the authors reported 418 notifications, of which 181 adults were deemed to harbor a definite intracranial vascular malformation. The crude detection rate (per 100,000 adults per year) was 1.12 (95% CI: 0.90–1.37) for brain AVMs and 0.16 (95% CI: 0.08–0.27) for DAVFs. No cases with coexistence of DAVF and AVM were reported in this study, and the rate of incidental finding was 21% for AVM and 15% for DAVF.[4]

In particular, the literature reported three cases of coexistent DAVF and AVM. One of these cases described a coexistent cranial DAVM and AVM, sharing the same drainage route.[6] The authors described a 63-year-old female symptomatic for seizures, where DSA showed bilateral DAVFs in the anterior cranial fossa and AVM in the left frontal lobe. A dilated vein with large varix was the common drainer of both the left DAVF and the AVM. The patient was surgically treated for both the vascular malformations. Two past cases were reported of the coexistence of DAVF and AVM. The first case was reported in 2012[7] in a 7-year-old boy, but the AVM was de novo constituted after embolization of a DAVF (supplied by the right pericallosal artery and drained into the medial parietal vein which dilated and flowed to the superior sagittal sinus), together with multiple DAVFs. The DAVFs were fed by the bilateral MMA, bilateral OA, bilateral posterior meningeal arteries, tentorial branches of bilateral posterior cerebral arteries, and superior cerebellar arteries; venous drainage occurred via a dilated meningeal vein (which looked like the superior sagittal sinus), torcular Herophili, straight sinus, Rosenthal basal vein, superior petrosal sinus, sphenoparietal sinus, and cortical veins to the cavernous sinus. The AVM was located at the left medial occipital lobe and was supplied by branches of the right pericallosal artery and drained to the dilated meningeal vein through the right medial parietal vein. The authors attributed the AVM formation to the hemodynamic change after the embolization of the presenting DAVF. Sattur et al.[8] reported the case of a 56-year-old male harboring a large, acute right temporal intracerebral hemorrhage (ICH). DSA revealed a high-grade parasagittal DAVF with cortical venous reflux close to a prior craniotomy site for glioma. After endovascular embolization of the DAVF and surgical evacuation of the ICH, a 7-month follow-up DSA showed a high-flow, right superior temporal cortical AVM together with the incomplete embolization and progression of the DAVF. The patient was surgically treated for both the vascular malformations.

The proposed case presented differs from the three available in the literature because the coexistence of DAVF and AVM refers to two findings, both incidental, but not correlated with each other. Instead, in the three cases previously described the causal relationship between DAVF and its incomplete treatment and AVM is clearly evident, so they cannot be considered two independent findings. Furthermore, in all three cases, they were not incidental findings, but clearly symptomatic. As previously outlined, the presented case shows the extremely uncommon association of two uncommon vascular malformations (DAVF and AVM) as incidentally discovered and asymptomatic disease. In addition, they are independent each from the other and not etiologically related, being these features not previously reported in the few published cases that were discussed.

In the therapeutic dilemma of three different vascular diseases in the brain of the same patient, we chose to treat the atheromatous stenosis of the right MCA with medical therapy, to embolize the DAVF, whose risk profile was conditioned in particular by the characteristics of the occipital drainage vein,[9] and not to treat in any way but to subject to follow-up the small pial AVM, asymptomatic and located in an area difficult to surgically approach.

Conclusions

Although rare and not previously reported, the coexistence of independent DAVF and AVM may occur, even as an incidental finding. In particular, the diagnostic management of acute stroke is mainly focused on the selection of patients for IVT and EVT, and unrelated conditions may be present but missed. Therefore, a systematic vascular evaluation is warranted, even in acute stroke patients, and eventually considered and deferred after the acute treatment. In some cases, incidental findings may complicate the therapeutic decisions, in particular when guidelines or evidence are not present in the literature. In these cases, an individual and multidisciplinary evaluation of the risk-to-benefit ratio for each therapeutic choice for each finding should be recommended, potentially affecting the stroke treatment too.

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Marialuisa Zedde and Rosario Pascarella. The first draft of the manuscript was written by Marialuisa Zedde and Rosario Pascarella. All authors read and approved the final manuscript, met the requirements for authorship, and believe that the manuscript represents honest work.

Ethical policy and institutional review board statement

Not applicable.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient has given his consent for his images and other clinical information to be reported in the journal. The patient understands that his name and initials will not be published and due efforts will be made to conceal his identity, but anonymity cannot be guaranteed.

Data availability statement

Data sharing is not applicable to this article as no datasets were generated and/or analyzed during the current study.

Conflicts of interest

There are no conflicts of interest.

Funding Statement

Nil.