Tentorial Dural Arteriovenous Fistulas as a Cause of Thalamic Edema: 2 Cases of an Important Differential Diagnosis to Consider

Abstract

The differential diagnosis for bilateral thalamic edema is extensive and includes vascular, neoplastic, metabolic, and infectious causes. Of the vascular causes of thalamic edema, arterial and venous infarctions are well-documented, but dural arteriovenous fistulas (dAVFs) are a relatively uncommon and widely underrecognized cause of thalamic edema. Dural AVFs are notoriously difficult to diagnose clinically, especially in the absence of hemorrhage, and cross-sectional imaging findings can be subtle. This can result in a delayed diagnosis, and occasionally, an invasive biopsy for further clarification of a purely vascular disease. In this review, we detail our experience with the imaging diagnosis of dAVF as a cause of thalamic edema and present a short differential of other vascular causes.

Introduction

Case Reports

Case 1

A 65-year-old man was evaluated at an outside hospital for recent cognitive changes. Per his wife, he had been acting “off,” sleeping through most of the day, and overall seemed “down and depressed.” His cognitive changes worsened, and his conversations stopped making sense. He presented at an outside hospital emergency department (ED) after his wife found him trying to use a razor to comb his hair. A head computed tomography (CT) was done, which was reportedly normal. A brain magnetic resonance imaging (MRI) performed during the same visit showed expansile bithalamic lesions, reportedly concerning for lymphoma or other malignancy (Figure 1A). He was admitted to the hospital and underwent a brain biopsy, which showed no definite evidence of tumor. A repeat biopsy was recommended by the outside facility, but the patient was transferred to our institution for a second opinion.

Figure 1.

A 65-year-old man with bithalamic edema from dural arteriovenous fistula (dAVF). A, An axial fluid attenuation inversion recovery (FLAIR) sequence showing expansile signal abnormality in the left greater than right thalamus, with prominent enhancement (B) and no restricted diffusion on the apparent diffusion coefficient (ADC) maps (C). D, An axial FLAIR sequence showing postbiopsy changes in the left thalamus (arrow), which showed reactive changes without evidence of malignancy. E, A time-of-flight magnetic resonance (MR) angiography which showed possible arterialized flow in the straight sinus. F, A lateral view digital subtraction angiography in the late arterialized phase, showing early venous drainage into the vein of Galen related to a dAVF (arrow).

A repeat MRI at our hospital showed bithalamic edema, and postbiopsy changes in the left thalamus (Figure 1). There was associated prominent patchy enhancement within the areas of edema, without restricted diffusion (Figure 1). Due to the pattern of thalamic edema, there was concern for a vascular lesion, and an MRA was performed. The MRA showed abnormal flow-related enhancement in the straight sinus, concerning for a dural arteriovenous fistula (dAVF; Figure 1). A conventional cerebral angiogram was recommended and showed a tentorial dAVF with supply from the posterior meningeal branch of the posterior cerebral artery (PCA), with retrograde venous drainage into the vein of Galen and reflux into the superior cerebellar and superior vermian veins, Cognard IIa + b (Figure 1). The fistula was disconnected via a midline occipital craniotomy and microsurgical clipping. Postoperative angiogram showed no residual arteriovenous shunting, and the patient’s cognition markedly improved over a few weeks.

Case 2

A 52-year-old man was brought into the ED by his wife for mental status changes with 2 weeks of increased somnolence, urinary incontinence, and confusion. At presentation to the ED, he was lethargic but arousable. He had no focal neurological deficits and could follow simple commands but was unable to follow more complex commands.

A noncontrast head CT was performed and showed an area of hypoattenuation in the left thalamus (Figure 2). Subsequent MRI showed edema in the left greater than right thalamus, with areas of restricted diffusion and small foci of patchy enhancement (Figure 2). This raised concern for venous sinus thrombosis. Computed tomography venogram (suboptimally timed) showed arterial enhancement of the vein of Galen with small size or chronic thrombosis of the straight sinus (Figure 2). There was also unusual tortuosity of the basal veins of Rosenthal. A conventional angiogram was recommended for further evaluation and showed a tentorial dAVF, with a meningeal branch of the P1 segment of the right PCA (artery of Davidoff-Schechter) draining directly into the proximal straight sinus (Figure 2). There was retrograde flow into the deep cerebral venous system (Cognard IIa). The fistula was successfully embolized with ethylene-vinyl copolymer suspended in dimethyl sulfoxide and opacified with tantalum (Onyx, eV3). The patient’s cognition improved over the next 2 months, with return back to cognitive baseline.

Figure 2.

A 52-year-old man with bithalamic edema from dural arteriovenous fistula (dAVF). A, An axial noncontrast computed tomography (CT) showing edema in both thalami, better depicted on the axial fluid attenuation inversion recovery (FLAIR) sequence (B). There is only mild associated enhancement on the postcontrast sequence (C). D, A sagittal maximum intensity projection image from a CT angiogram showing arterialized flow in the straight sinus. Early to mid arterial phase lateral digital subtraction angiography (DSA) from an internal carotid artery injection shows early venous drainage into the straight sinus (arrow, E). Lateral DSA from the external carotid artery injection more clearly shows early venous drainage into the straight sinus from a dAVF (F).

Discussion

The differential diagnosis for thalamic edema is broad and includes malignancy, infection, toxic/metabolic, and vascular causes. Vascular causes include arterial infarction, venous thrombosis, vascular malformations, and atypical posterior reversible encephalopathy syndrome (PRES). Dural AVF is also part of that differential but is an uncommon and under recognized cause of thalamic edema.^1,2 In fact, dAVFs are usually not listed in the classic radiologic differential diagnosis for thalamic lesions published in prominent radiology journals,^3-5 which is likely due to the relative rarity of dAVFs and also the difficulties of making the diagnosis of a dural fistula on cross-sectional imaging. In several case series performed at academic institutions, it has been noted that there is often a significant delay in diagnosis due to lack of recognition of this entity by the clinical team.^1,2 The imaging findings of tentorial dAVF may be incorrectly attributed to straight sinus thrombosis (which in it’s chronic form, may be coexistent with a dAVF), and patients are placed on anticoagulation therapy. It is only after patients fail to respond to anticoagulation therapy that the diagnosis of a dAVF is entertained. In another publication, one patient had 3 recurrent episodes of thalamic edema and hemorrhage before the diagnosis of a fistula was made.⁶ It is likely that this condition is underdiagnosed in the general community and globally as well. The goal of our review is to discuss the vascular causes of thalamic edema and to review their respective imaging findings, with an emphasis on dAVF as an entity that should be included in the differential diagnosis of bithalamic edema. A working knowledge of these findings on the part of radiologists and clinicians can lead to a timely and accurate diagnosis.

Blood Supply and Venous Drainage of the Thalamus

Any discussion of vascular pathology involving the thalamus requires an understanding of the blood supply to the thalamus. Briefly, the arterial blood supply of the thalamus is classically divided into 4 territories: anterior, paramedian, inferolateral, and posterior.⁷ The anterior territory is supplied by the tuberothalamic artery, a branch of the posterior communicating artery.⁸ The paramedian territory is supplied by thalamoperforators, which arise from the P1 segment of the PCA. The inferolateral territory is supplied by the thalamogeniculate arteries, which arise off of the P2 segment of the PCA, and the posterior segment is supplied by the posterior choroidal arteries, which also arise from the P2 segment of the PCA.⁸

The venous drainage of the thalamus is mainly via the deep venous system. The septal and thalamostriate veins drain the basal ganglia to various degrees, and they unite to form the internal cerebral vein. The thalamostriate vein is not the main draining vein of the thalamus, despite its name. The thalamic veins drain into the internal cerebral vein and basal vein of Rosenthal, to various degrees. The internal cerebral vein then unites with the basal vein of Rosenthal, which together with the contralateral deep venous system, merge to form the vein of Galen. The vein of Galen and inferior sagittal sinus unite to form the straight sinus, which drains into the torcula Herophili.

Dural AVF

Tentorial dAVFs are often an overlooked cause of thalamic edema. Cross-sectional imaging findings may be extremely subtle, and thalamic edema from venous congestion may be the only finding. Patchy areas of restricted diffusion or enhancement due to venous infarction or hemorrhage may also be present. Computed tomography angiography may show abnormally increased vascularity, with an increased number, size, or tortuosity of vessels, a clue to the diagnosis of a dAVF. An arterially enhancing vein may also be evident on a well-timed CT angiogram (CTA), which strongly suggests the presence of a vascular shunt lesion. Computed tomography venogram is often performed as part of the evaluation for thalamic edema and may show chronic thrombosis of a portion of the deep venous system.¹ Chronic dural sinus thrombosis has been implicated in the formation of dAVFs.⁹ In the setting of tentorial dAVFs with thalamic venous edema/infarcts, it is the authors’ experience that there is often partial or complete thrombosis of the straight sinus, potentially as the underlying cause of the fistula. Presenting symptoms can include thalamic dementia, with progressive cognitive dysfunction that includes deficits in executive function, attention, memory, and disorientation.¹ Aphasia, ataxia, or focal neurologic deficits may also be present.¹ Patients may be started on anticoagulation for incomplete diagnosis of dural venous thrombosis, which could potentially put them at higher risk of venous hemorrhage in the setting of elevated venous pressures from the fistula. As in case 1, the patient may also undergo invasive biopsy if the signal abnormalities in the thalamus are mischaracterized as a tumor.

Deep Venous Sinus Thrombosis

Thrombosis of the deep venous drainage system can cause venous stasis and vasogenic edema in the basal ganglia and thalami, which if untreated, could progress to venous ischemia or hemorrhage.¹⁰ Unlike arterial infarcts, the edema in the thalamus does not correspond to any vascular territory and tends to involve the entire thalamus. The imaging findings can look identical to tentorial dAVF given that the pathophysiology (venous hypertension) of the parenchymal findings is the same. On noncontrast CT, abnormal hyperattenuation of a deep vein with or without thalamic edema may be the only finding (Figure 3). Conventional MRI sequences may show intrinsic T1 hyperintensity within the thrombosed sinus, reflecting methemoglobin. Blooming hypointensity within the sinus may be present on gradient recalled echo imaging or susceptibility-weighted imaging. Magnetic resonance venography or CT venogram is frequently definitive. Magnetic resonance venogram will show loss of the normal/expected flow-related hyperintensity within the sinus. Computed tomography venography will show a filling defect within the sinus, representing thrombus.¹¹ High-risk features that may suggest the presence of a dAVF include enlarged or tortuous cerebral veins or external carotid artery branches and absent or small dural veins with chronic thrombosis. Cases suspected of harboring a dAVF can be further evaluated with conventional cerebral angiography prior to initiating anticoagulation.

Figure 3.

Dural sinus thrombosis in a young patient with headaches. A, An axial noncontrast computed tomography (CT) showing edema in the left greater than right thalamus. B, At the level of the corona radiata shows hyperdensity within the straight sinus, concerning for deep venous thrombosis, which was confirmed on subsequent CT venogram (arrow, C).

Arterial Occlusions

The classic arterial cause of bilateral paramedian thalamic infarction is an artery of Percheron infarct. In this clinical entity, the arterial supply to both paramedian thalami is derived from a single arterial pedicle arising from a P1 segment. Occlusion of this artery results in bilateral thalamic infarcts (Figure 4). Additional infarcts may also be seen in the interpeduncular fossa of the rostral midbrain or the anterior thalamus.¹¹ The edema is usually well-demarcated, corresponding to the arterial territory involved. The other important differential diagnosis for artery of Percheron infarction is top of the basilar occlusion, which tends to involve the very proximal bilateral P1 segments with occlusion of bilateral thalamoperforators. Computed tomography angiogram or MRA is key for differentiating between the 2 entities, as a normal basilar artery argues against top of the basilar syndrome and suggests an artery of Percheron infarction. The thalamoperforators are not consistently visualized on CTA or MRA, even when normal. Differentiating features between thalamic arterial infarcts and venous congestion from dAVF or venous thrombosis includes strong restricted diffusion corresponding to a known arterial territory for arterial infarcts and prominent vasogenic edema in the thalamus that does not correspond to arterial territory for venous infarcts.

Figure 4.

Artery of Percheron infarct in an 87-year-old man with altered mental status. A, An axial diffusion-weighted image of the brain showing acute infarcts in both thalami (arrows). B, An axial diffusion-weighted image of the brain at the level of the cerebral peduncles, showing acute infarction of the mid brain (arrow). C, A coronal maximum intensity projection image from a computed tomography angiogram (CTA) performed an hour prior to the magnetic resonance imaging (MRI), showing wide patency of the basilar artery without thrombosis. The distribution of infarcts on MRI and patent basilar artery on CTA are consistent with an artery of Percheron infarct.

Posterior Reversible Encephalopathy Syndrome

Fairly symmetric reversible vasogenic edema in the bilateral parieto-occipital lobes is the imaging hallmark of PRES. However, PRES can present in other parts of the brain, with little or no signal abnormality in the posterior cerebral hemispheres.¹² The incidence of PRES in the thalamus was found to be 30% in one large study.¹² Other areas of involvement include the basal ganglia, pons, and cerebellar hemispheres, the so-called “central variant PRES.”¹³ Thalamic PRES remains a diagnosis of exclusion given the other vascular etiologies that can cause edema in this region (Figure 5). In addition to vasogenic edema, hemorrhage, restricted diffusion, and mild enhancement may occasionally be seen in association with the lesions of PRES.¹⁴ When present, these features can further confound the diagnosis.

Figure 5.

Posterior reversible encephalopathy syndrome (PRES) in a patient with severe hypertension and a history of medical noncompliance. A, Edema in the right greater than left thalamus. Edema is also present in the pons and bilateral cerebellar white matter (B and C, respectively). There was no associated contrast enhancement or restricted diffusion. Vascular imaging did not show dural sinus thrombosis or evidence of arteriovenous shunting or fistula.

Other

Arteriovenous malformations and cavernous malformations located in the thalamus can also result in edema after a recent hemorrhage, but the diagnosis is usually clear on imaging. Arteriovenous malformations typically have a nidus with associated flow voids and enhancing vessels. Cavernous malformations usually show a rounded lesion with internal heterogeneous signal on T1- and T2-weighted sequences and a complete hemosiderin ring surrounding the lesion. An adjacent developmental venous anomaly may also be seen in the vicinity of the cavernous malformation but is not required for the diagnosis. Hypoxic ischemic brain injury is another cause of thalamic edema, but there is usually evidence of restricted diffusion/cytotoxic edema in at least one other part of the brain such as the cerebral cortex, basal ganglia, or hippocampus. The clinical history and patient presentation in hypoxic ischemic encephalopathy is also strongly suggestive, usually with a recent cardiac/respiratory arrest or overdose syndrome (Figure 6).

Figure 6.

Anoxic brain injury in a 65-year-old found down in cardiac arrest. A, Abnormal fluid attenuation inversion recovery (FLAIR) signal in both thalami, as well as the caudate heads, putamina, and cerebral cortices. Diffusion-weighted imaging (DWI) and ADC maps (B and C) shows associated restricted diffusion in the areas of signal abnormality, consistent with cytotoxic edema.

Diseases outside the vascular category may also result in bithalamic lesions and should be remain on the differential. These include tumors (lymphoma, high-grade gliomas), infections (toxoplasmosis, flavivirus), and toxic/metabolic causes (osmotic myelinolysis, Wilson disease, Wernicke encephalopathy).³

Conclusion

Dural arteriovenous fistulas are a widely under recognized cause of unilateral or bilateral thalamic edema. Given the relatively subtle vascular findings and the absence of this entity in the typical imaging differential diagnosis for thalamic signal abnormality, this can be a difficult diagnosis to make. Vascular imaging with CT/MR angiogram and venography (Figure 7) should be considered in all patients who present with bilateral thalamic edema, especially in the older age groups in which dAVFs are more common.

Figure 7.

Contrast-enhanced magnetic resonance (MR) showing normal intracranial venous anatomy. This is a maximum intensity projection of a sagittal postcontrast image of the brain, depicting the intracranial venous anatomy. The blue arrow is the internal cerebral vein, the arrowhead shows the vein of Galen, the curved arrow shows the straight sinus, the dashed arrow shows the torcular Herophili, the star shows the inferior sagittal sinus, and the double-headed arrow shows the superior sagittal sinus.