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When formation of cerebral vasculature goes aberrant – A pictorial essay
Samarth R Shah1, Amol A Gautam2, Asif I Tamboli1, Amol S Bhoite1
1 Department of Radiodiagnosis, Krishna Institute of Medical Sciences, Deemed to be University, Karad, Satara, Maharashtra, India
2 Department of Radiodiagnosis, Symbiosis Medical College for Women, Pune, Maharashtra, India
| Date of Submission | 27-Aug-2022 |
| Date of Decision | 31-Oct-2022 |
| Date of Acceptance | 03-Nov-2022 |
| Date of Web Publication | 14-Mar-2023 |
Correspondence Address:
Samarth R Shah,
Department of Radiodiagnosis, in KIMSDU, Karad, Maharashtra
India
 Source of Support: None, Conflict of Interest: None DOI: 10.4103/mjdrdypu.mjdrdypu_756_22
Vascular malformations of the brain are aberrant vascular connections that are most likely congenital. Cerebral vascular malformations are the umbrella term for multiple conditions, each with different symptoms, signs, and imaging characteristics. These conditions are (1) Arteriovenous malformations, abnormal arteries, and veins; (2) Dural arteriovenous fistula; (3) Developmental venous anomalies; (4) Cavernous malformations, enlarged blood-filled spaces; (5) Cavernous angiomas, abnormal veins; (6) capillary telangiectasias, enlarged capillary-sized vessels; (7) vein of Galen malformations; and (8) mixed malformations. It is important to study the complications of each and their mimics to make an accurate diagnosis. Various imaging features of different vascular malformations seen on MRI are discussed that which would aid in diagnosis and planning management.
Keywords: Arterio-venous, capillary telangiectasia, carotid cavernous fistula, cavernous angioma, developmental venous anomaly, vascular malformations, a vein of Galen
How to cite this URL:
Shah SR, Gautam AA, Tamboli AI, Bhoite AS. When formation of cerebral vasculature goes aberrant – A pictorial essay. Med J DY Patil Vidyapeeth [Epub ahead of print] [cited 2023 Mar 24]. Available from: https://www.mjdrdypv.org/preprintarticle.asp?id=371650 |
| Introduction | |  |
Arteriovenous malformations (AVMs) are vascular system developmental aberrations that is made up of tangles of terribly formed blood vessels where the feeding arteries are joined to the venous drainage network directly, without any intervening capillary system.[1],[2],[3],[4],[5]
Although the exact cause of brain AVMs is unknown, it is likely multifactorial, with both genetic mutation and angiogenic stimulation—the physiological process that causes preexisting blood vessels to grow new blood vessels—appearing to play a part in AVM development. Others argue that the primary cause of these kinds of strokes, is an angiopathic reaction to either cerebral ischemia or hemorrhagic event.[1],[6],[7],[8],[9]
The majority of CVMs are congenital lesions caused by morphogenetic abnormalities in the arteries, capillaries, veins, or a mix of these structures. Development of the human fetal vascular system occurs via two related processes: vasculogenesis and angiogenesis. In vasculogenesis, capillary-like tubes develop first and constitute the primary vascular plexus. This primary capillary network is subsequently remodelled into large-caliber vessels (arteries, veins) and small capillaries. Angiogenesis is regulated by a number of intercell signaling and growth factors. The development of several CVMs has been linked to mutations in various components of the angiogenetic system.
Cerebral vascular malformations can be classified in various ways, based on high or low-flow malformations, whether or not arteriovenous shunting is seen, and according to histopathological findings.[1]
[Table 1]. High or low-flow cerebral vascular malformations.[1]
[Table 2]. Functional classification: With or without AV shunting.[1]
| Case Descriptions | | |
AV malformations
AVMs are the most prevalent vascular malformations of the brain. The mortality rate is 10-15% of patients who have a hemorrhage, and morbidity varies from approximately 30-50%. There is no sex predilection. Despite the considered congenital origin of AVMs, the clinical presentation most commonly occurs in young adults.
AVMs are composed of a central vascular nidus which is a conglomerate of arteries and veins. There is no intervening capillary bed, and the feeding arteries drain directly into the draining veins by one or multiple fistulae. These arteries lack the normal muscular layer and the draining veins often appear dilated due to the shunted high-velocity arterial blood flow entering through the fistulae.
AVMs cause neurological dysfunction through the following three possible pathophysiological mechanisms. Firstly, the abnormal blood vessels have the propensity to bleed resulting in hemorrhage occurring in the subarachnoid space, the intraventricular space, or, more commonly in the brain parenchyma. Secondly, in the absence of hemorrhage, seizures may occur as a consequence of the mass effect of AVM or venous hypertension in draining veins. The third important cause of slowly progressive neurological deficits is attributed to the "steal phenomenon" which is thought to be related to normal brain parenchyma deprivation from nutrients and oxygen, as blood bypasses the normal capillary bed to the malformed arteriovenous channels.
Cerebral AVMs are the most common symptomatic vascular malformations. Seen incidentally in 15% of asymptomatic patients. Can present with seizures, headaches, ischemic events due to vascular steal from the normal brain, or hemorrhage.
They are a direct shunt between an artery and a vein with multiple thin vessels (nidus) connecting the two without any evidence of a capillary bed.[11],[12]
There are two types of aberrant vascular networks that can be found if a nidus is present. The glomerular or compact type nidus is the most common, consisting of aberrant vessels with no interspersed normal brain tissue. The so-called diffuse or proliferative type nidus, in which brain parenchyma is distributed throughout the tangle of arteries, is a less common second kind.
Although brain AVMs are congenital, patients usually present later in life, with intracranial hemorrhage or seizures as the most prevalent symptoms.[14],[15],[16],[17]
Most of them are parenchymal (pial), and supratentorial and are seen as solitary lesions.
The diagnostic criteria include (a) cross-sectional imaging or conventional angiography revealing the existence of a nidus embedded within the brain parenchyma; and (b) early venous drainage, which is best seen in dynamic studies.
The Spetzler-Martin AVM grading system assigns points to various angiographic aspects of intracranial AVMs to provide a score that predicts the probability of surgical morbidity and mortality. Minimum grading (I) to maximum grading (V).
[Table 3]. Spetzler-Martin arteriovenous malformation (AVM) grading system. | Table 3: Spetzler-Martin arteriovenous malformation (AVM) grading system
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IMAGING: (BAG OF WORMS)
MR
Tightly packed mass or honeycomb of flow voids – T1WI & T2WI as they are high flow lesions.
Gliotic brain parenchyma within an AVM is hyperintense on T2WI & FLAIR.
GRE – blooming (Haemorrhagic residua).
MR ANGIOGRAPHY
Dilated and tortuous feeding arteries with a tightly packed tangle of abnormal arteries and veins with no intervening capillary bed/brain parenchyma and early draining enlarged, tortuous vein.
Case 1: The case of a 59-year-old male who presented with frequent headaches of insidious onset for five years moreover on the left side without any seizures or weakness.
a) and b) Multiple enlarged Serpiginous entangled vascular channels exhibiting flow voids on T2 and FLAIR sequences in the left parieto-occipital region (parenchymal) comprising both arterial and venous channels with dilated cortical veins along the cortex. Nidus is seen containing gliotic brain parenchyma. Nidus is 48 x 40 x 36 mm (Diffuse/Proliferative type) with evidence of gliosis of intervening brain parenchyma. Arterial feeders are from the left PCA and a few fibers from cortical branches of the left MCA with venous drainage to the posterior part of the superior sagittal sinus and straight sinus.
c) Blooming in vascular channels on gradient images. No evidence of previous hemorrhage, intranidal aneurysm, ectasia, or stenosis of drawing veins.
d) and e) MR Angio sequence and f) Contrast Venous sequence show artery venous malformation in left occipito-parietal lobe with supplying artery – left PCA and cortical branches of left MCA and venous drainage to straight sinus and posterior superior sagittal sinus via superficial cortical veins.
f) Contrast Venous sequence shows a nidus in the parieto-occipital region with shunting between the branches of PCA and the cortical veins.
Findings suggestive of Spetzler Martin grade III AVM [Figure 1]. | Figure 1: Case 1: (a) T2 (b) FLAIR sequences showing flow voids (arrow) on in the left parieto-occipital region with dilated cortical veins along cortex. Nidus is seen containing gliotic brain parenchyma. (c) Blooming in vascular channels on GRE (arrow). (d and e) MR Angio sequence and (f) Contrast Venous sequence show AVM (arrow) in the left occipito-parietal lobe. (f) Contrast Venous sequence shows a nidus in the parieto-occipital region (arrow) with shunting between the branches of PCA and the cortical veins
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Case 2: Case of a 51-year-old female who presented with insidious onset headaches for two years and frequent episodes of giddiness for three to four years. No evidence of weakness or seizures.
T2 (a) and FLAIR (b) sequences show multiple enlarged serpiginous areas of vascular flow void comprising arterial and venous channels noted in right frontal lobe (parenchymal). Nidus (compact) measures 26 x 23 x 21 mm. No evidence of gliosis within or around the nidus.
c) Blooming in the vessels on gradient images. No evidence of previous hemorrhage, intranidal aneurysm, ectasia or stenosis of draining veins.
d) MR Angio sequence shows branches of MCA seen communicating with the nidus.
e) Contrast Venous sequence shows a nidus in the frontal region with shunting between the branches of MCA and the cortical veins. Arterial feeders are from the right ACA & MCA and venous drainage to the superior sagittal sinus through superficial cortical veins.
Findings suggestive of Spetzler Martin grade I AVM [Figure 2] | Figure 2: Case 2: T2 (a) FLAIR (b) sequences show flow voids (arrow) in the right frontal lobe with nidus. (c) GRE sequences show blooming (arrow). (d) MR Angio sequence show branches of MCA (arrow) seen communicating with the nidus. (e) Contrast Venous sequence shows a nidus in the frontal region with shunting between the branches of MCA and the cortical veins (arrow)
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Case 3: Case of a 37-year-old female who presented with complaints of headaches and giddiness for two years. No evidence of weakness or seizures.
a) and b) Multiple flow voids were noted on T2 and FLAIR sequences in the right parietal region with dilated cortical veins along the cortex. Nidus is seen containing gliotic brain parenchyma.
c) Blooming on gradient images.
d) MR Angio sequence show branches of MCA seen communicating with the nidus and early draining cortical veins.
e) Contrast Venous sequence shows a nidus in the parietal region with shunting between the branches of MCA and the cortical veins.
Findings suggestive of Spetzler Martin grade I AVM [Figure 3] | Figure 3: Case 3: (a) and (b) Multiple flow voids (arrow) noted on T2 and FLAIR sequences in the right parietal region with dilated cortical veins along the cortex. Nidus is seen containing gliotic brain parenchyma. (c) Blooming (arrow) on gradient images. (d) MR Angio sequence show branches of MCA seen communicating with the nidus and early draining cortical veins (arrow). (e) Contrast Venous sequence shows a nidus in the parietal region with shunting between the branches of MCA and the cortical veins (arrow)
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Dural AV fistulas
About 10%–15% of cerebral vascular malformations are intracranial dural arteriovenous fistulas (DAVFs), which are a network of abnormal contacts between dural arteries and dural venous sinuses or cortical veins without an intervening capillary network or nidus.[13],[18],[19]
There is evidence that many are caused after a dural sinus thrombosis, trauma, infection, or prior craniotomy. Those DAVFs involving the larger brain veins usually arise from progressive narrowing or blockage of one of the brain's venous sinuses, which route circulated blood from the brain back to the heart.
The main abnormality in DAVFs is a connection between the dural arteries and veins within the venous sinus wall via small vessels that are approximately 30 micrometers on average. In those patients with a provoking event, neovascularization is induced by a previously thrombosed dural venous sinus, typically the transverse sinus.
They are the second most common cerebral vascular malformations with AV shunting. These are tiny crack-like vessels that shunt blood b/w meningeal arteries and small venules within the dural sinus wall.[9] Usually in Transverse Sinus (adults) and Superior sagittal sinus (Children) of varying sizes.
The simplest method to categorize these lesions is to divide them among those that have cerebral venous reflux and those that do not. The latter are benign fistulas (Borden type 1) that seldom cause neurologic impairments, whereas the former are malignant fistulas (Borden types 2 and 3).[10],[11]
Symptom onset may be sudden or gradual, with our patients' presentations ranging from sudden onset of nausea and vomiting to gradually progressive tetraparesis.[18],[19],[20],[21],[22],[23]
Headache, nausea/vomiting, tinnitus, intracranial bleeding, seizures, dementia, altered consciousness, and focal non-hemorrhagic neurologic symptoms are all common symptoms of malignant dural AVFs, which are caused by venous congestion or venous pouch rupture.[24],[25]
IMAGING:
MRI
Dilated cortical veins without nidus adjacent to the normal appearing brain.
Most common finding – is thrombosed dural venous sinus with flow voids.
Thrombus – T1 and T2 isointense and typically T2* - blooming.
ANGIOGRAPHY
Best imaging tool.
DSA with super-selective catheterization of dural and transosseous feeders required.
Dural branches arising from ECA, ICA, and vertebral arteries.
Presence of dural sinus thrombosis, flow reversal with drainage into cortical veins, and engorged tortuous pial veins.
Case 4: Case of a 54-year-old male who presented with complaints of headaches for four years with the blurring of vision for one year without any history of seizure or weakness. No evidence of dementia or altered behavior.
a) and b) Area of altered signal intensity noted in left occipital lobe with multiple flow voids noted on T2 and FLAIR sequences. Numerous extensive prominent and tortuous dural varicosities were noted predominantly near left transverse sinuses.
c) Blooming on gradient images.
d) MR Venogram sequence shows Numerous and extensive prominent and tortuous dural varicosities noted predominantly near left transverse sinuses.
Findings suggestive of Dural AV fistula [Figure 4] | Figure 4: Case 4: (a) and (b) T2 and FLAIR sequences show an area of altered signal intensity (arrow) noted in the left occipital lobe with multiple flow voids. Numerous extensive prominent and tortuous dural varicosities (arrowhead) were noted predominantly near the left transverse sinuses. (c) Blooming (arrow) on gradient images. (d) MR Venogram sequence shows Numerous and extensive prominent and tortuous dural varicosities (arrow) noted predominantly near left transverse sinuses
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Carotid-Cavernous Fistula
A carotid-cavernous sinus fistula is an anomalous connection between veins and arteries in the cavernous sinus.
Direct CCFs are thought to develop as a result of an iatrogenic injury following an endovascular intervention or a trans-sphenoidal operation, an acceleration-deceleration force from a traumatic injury, or a traumatic tear in the artery from a skull base fracture (see figure). They can also develop on their own following the rupture of an ICA aneurysm or artery weakness brought on by a hereditary disease.
Indirect CCFs happen when the carotid artery's dural branches burst due to weakness brought on by comorbidities like hypertension or defects like hereditary conditions. According to a different view, the danger of the dural arteries rupturing increases as the cavernous sinus pressure rises after thrombosis.[26],[27],[28],[29]
AV shunting developing within the cavernous sinus. It is almost always acquired.
[Table 4]. Can be of two types: Direct or indirect.
[Table 5]. Classified into four types (Barrow classification).
Can present with pulsatile exophthalmos, chemosis and subconjunctival haemorrhage, proptosis, progressive visual loss, pulsatile tinnitus (usually objective), raised intracranial pressure, subarachnoid hemorrhage, intracerebral hemorrhage, otorrhagia, epistaxis, cranial nerve (III, IV, Vc, VI) palsies.[14]
On imaging;
CT FINDINGS consist of Mild or striking proptosis, Prominent cavernous sinus, Enlarged SOV and EOM, "Dirty" fat secondary to edema and venous engorgement, Subarachnoid hemorrhage from trauma or ruptured cortical veins.
On CECT scans, Enlarged SOV and CS with Inferior drainage into a prominent pterygoid venous plexus and posterior drainage into the clival venous plexus.
On MRI
Bulging SOV and CS with flow voids on T1W and asymmetric flow- related signal loss in the affected veins on T2W.
An ultrasound would show normal flow in the SOV from extra- to intracranial (i.e., from orbit into cavernous sinus). Using Doppler US, flow reversal (intracranial to extracranial) within an expanded SOV can be proven noninvasively.
[Table 6]. Angiography Findings.
Case 5: Case of a 37-year-old female with mild proptosis of a left eye for three months, blurring of vision, and subconjunctival hemorrhage for two to three months.
a) and b) Asymmetrically dilated & tortuous left superior ophthalmic vein and dilated left half of the cavernous sinus with T2 flow void within.
c) Large partly thrombosed aneurysm noted in the cavernous segment of left ICA measuring (~ 15 x 11 mm) which is bulging along medial & lateral margin of the left cavernous sinus.
High flow communication between the intracavernous portion of the left ICA and the left cavernous sinus was also noted. Suggestive of Carotico-cavernous fistula (Direct-Barrow type A) [Figure 5] | Figure 5: Case 5: (a) Dilated left half of the cavernous sinus with T2 flow void within (arrow) and (b) Asymmetrically dilated and tortuous left superior ophthalmic vein (arrow). (c) Large partly thrombosed aneurysm noted in the cavernous segment of left ICA (arrow) bulging along medial and lateral margin of the left cavernous sinus. High flow communication between the intracavernous portion of the left ICA and the left cavernous sinus was also noted
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| Developmental Venous Anomaly | | |
Most commonly encountered cerebral vascular malformations at autopsies. They are assumed to be anatomic variants originating from prenatal cortical venous drainage maldevelopment, most likely due to the recruitment of parenchymal veins to compensate for the loss or disappearance of a section of the cerebral venous system.
DVAs are congenital malformations without artery or capillary components but with angiogenically developed venous walls. They are made up of radially oriented, swollen transcortical or subependymal collecting veins that connect to dilated medullary veins. These venous channels combine into a medically normal venous outflow tract, which is divided by normal intervening parenchyma.[30]
DVAs are characterized by larger medullary veins draining into a venous trunk that drains into a dural sinus or deep ependymal vein, giving the appearance of a "palm tree" or "caput medusa" on imaging. Typically, these lesions are solitary.
Patients are normally asymptomatic because the DVA is an imaging finding, but abrupt thrombosis of the collecting vein might cause bleeding or infarction.
On contrast-enhanced CT or MRI, the characteristic imaging finding of the caput medusa allows for easy diagnosis. The draining vein appears is attenuating to slightly hyperattenuating to the cortex on non-contrast CT, but if abruptly thrombosed, a substantially hyperattenuating vein may be detected. Depending on the magnitude of the flow voids, MR imaging may reveal them in the region of the medullary veins and draining veins. T2 hyperintensity in the vicinity of a DVA is occasionally found on MR imaging.
DVAs are "leave alone" lesions in the sense that resection causes venous infarction in the DVA-drained area.[19],[31],[32],[33],[34]
Case 6: Case of a 40-year-old female who presented with complaints of insidious onset headache for two to three years without a history of trauma. No evidence of seizure or ischemic attack.
On post-contrast T1WI (d), enlarged medullary veins are seen in the right gangliocapsular area (involving anterior portions of the external capsule, lenticular-striate nucleus, and internal capsule) with a characteristic "Medusa head" appearance draining into a single larger collecting vein which is directed inferno-medially towards the body of right lateral ventricle to drain into a deep ependymal vein – suggestive of Developmental venous anomaly. The above-mentioned collecting vein appears show a flow void on the T1 sequence (a). Additionally, a high T2/FLAIR signal is seen in the surrounding right gangliocapsular area not showing diffusion restriction or blooming – suggestive of partial gliosis (b & c) [Figure 6]. | Figure 6: Case 6: T1C+ (d) Enlarged medullary veins (arrow) are seen in the right gangliocapsular area with a characteristic "Medusa head" appearance draining into a single larger collecting vein (arrowhead) which is directed inferno-medially towards the body of right lateral ventricle to drain into a deep ependymal vein. The above-mentioned collecting vein appears show a flow void (arrow) on T1 sequence (a) T2/FLAIR hyperintensity suggestive of partial gliosis (arrow) (b and amp; c)
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Case 7: Case of a 40-year-old female who presented with complaints of giddiness & imbalance while walking for two years. CT scans done previously appeared unremarkable.
The area appears isointense on T1W (a), hyperintense on T2W/FLAIR (b), with no diffusion restriction and blooming on SWI sequence (c).
T1 contrast-venous study (d, e, f) shows subtle enhancement with medusa head appearance of prominent medullary veins converging in trans cortical collector vein.
Developmental venous anomaly with hemosiderin deposition [Figure 7] | Figure 7: Case 7: Altered signal intensity area (arrow) appearing isointense on T1W (a), hyperintense on T2W/FLAIR (b), with no diffusion restriction and blooming (arrow) on SWI sequence (c). T1 contrast-venous study (d-f) shows subtle enhancement with medusa head appearance (arrow) of prominent medullary veins (arrow) converging in transcortical collector vein (arrow)
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| Cerebral Cavernous Malformation | | |
Cavernous malformations (CM) are slow-flow vascular malformations. CMs are vascular hamartomas that consist of intercapillary vascular spaces of various sizes, sinusoids, and larger cavernous spaces with no intervening brain tissue.[35],[36]
These lesions are loaded with blood or thrombus and lack smooth muscular support. CM is connected with hemosiderin, whether or not they have visibly hemorrhaged, which may be related to ultrastructural investigations showing nonexistent or reduced tight connections. This indicates a localized breakdown of the blood-brain barrier and a reduction in vascular stability.
Patients may have seizures, localized neurologic impairments, or severe cerebral hemorrhage at the time of diagnosis, but the majority are asymptomatic.[37],[38],[39],[40]
IMAGING:
MR – DIAGNOSTIC
Focal central heterogeneity (varying hemorrhage within caverns)- POPCORN appearance on T2WI.
Circumferential hypointense ring of hemosiderin formed around high-intensity central areas.
Cerebral Amyloid Angiopathy or multiple hemorrhagic metastases are differentials in appropriate clinical settings and other relevant imaging findings.
[Table 7]. The Zabramski classification of cerebral cavernomas.
Case 8: Patient complained of facial twitching on the left side for 2 weeks. Area of altered signal (arrows) intensity appearing heterogeneously hyperintense on T1W (a) hypointense on T2WI/FLAIR (b and c), showing blooming on gradient images, hemo (d) and SWI (e) with corresponding hyperintensity on PHASE (f) in right precentral gyrus with fluid-fluid level and hypointense rim.
Findings suggestive of Cavernous hemangioma with hemorrhage (blood in subacute to the chronic stage) - Zabramski classification type II [Figure 8] | Figure 8: Case 8: Area of altered signal intensity (arrows) appearing heterogeneously hyperintense on T1W (a) hypointense on T2WI/FLAIR (b and c), showing blooming on gradient images, hemo (d) and SWI (e) with corresponding hyperintensity on PHASE (f) in right precentral gyrus with fluid-fluid level and hypointense rim
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| Vein of Galen Malformation | | |
It is an arteriovenous fistula that causes the median prosencephalic vein (MPV), the embryonic precursor of the vein of Galen, to dilate. The arteriovenous shunts associated with the MPV are thought to occur between 6 and 11 weeks of pregnancy.[41],[42] The enhanced flow through the MPV avoids the involuting of the transitory fetal venous drainage pattern. The straight sinus does not form in half of these people, and the vein drains into a falcine sinus. These lesions are more common in the newborn era and are the leading cause of noncardiac congestive heart failure in infants. A vascular steal can cause ischemic damage to the brain parenchyma.[43] They can appear later in infancy or even in adulthood on rare occasions. Older infants frequently have lesser cardiac symptoms and are brought to the doctor due to hydrocephalus caused by aqueduct or posterior third ventricle compression. Seizures are also possible. Headaches or subarachnoid haemorrhages can occur in both children and adults. Patients who present in the newborn period have a worse prognosis than those who present later in life. Males are more likely than females to have them, with a 2:1 ratio.
VOGM are classified as either choroidal or mural Multiple feeders from the pericallosal, choroidal, and thalmoperforating arteries feed the dilated venous pouch in the choroidal form, resulting in an extensive arterial network between the arterial feeders and the dilated venous pouch.
A dilated venous pouch is visible on CT imaging. Due to the compression of the Sylvius aqueduct by the mass effect of the dilated vein, hydrocephalus can occur. Vascular steal can cause parenchymal atrophy, and calcifications can result from ischemic brain injury. Intraventricular bleeding is a rare complication. Catheter angiography is still the gold standard for VOGM angioarchitecture evaluation. If a thrombus is present, T1 hyperintensity in the pouch may be observed on MR. In the case of ischemia or calcification, T1 hyperintensity might be found in the brain parenchyma. Diffusion may be reduced in the event of acute infarction. Diffuse brain destruction, often known as melting brain, can occur in severe situations.[44]
Case 9: Marked aneurysmal dilatation of the vein of the galen due to congenital AVM involving the medial prosencephalic vein. It measures (~ 46 x 37 x 33 mm). It exhibits a profound low signal on T2W (b) and T1W (a) sequences.
Dilated bilateral posterior cerebral artery branches, internal cerebral vein, Falcine sinus, straight sinus, and bilateral transverse and sigmoid sinuses.
Aneurysmal dilatation of the vein of Galen results in compression of the tectum and aqueduct of Sylvius and posterior 3rd ventricle with resultant marked dilatation on the 3rd and both lateral ventricles suggestive of acute obstructive hydrocephalus. Thinning of supra-tentorial brain parenchyma noted with a paucity of periventricular white matter and no evidence of periventricular ooze.
A signal misinterpretation on Phase (c) and SWI (d) with thrombus of varying ages in the periphery.
MR Angiogram (e) shows dilated feeding vessels entering the aneurysmal malformation.
Findings suggestive of Vein of Galen aneurysmal malformation – Mural type [Figure 9] | Figure 9: Case 9: Marked aneurysmal dilatation of vein of galen (arrow) exhibiting hypointensity on T2W (b) and T1W (a). Dilated bilateral posterior cerebral artery branches, internal cerebral vein, falcine sinus, straight sinus, bilateral transverse, and sigmoid sinuses. Acute obstructive hydrocephalus. Signal misinterpretation (arrow) on Phase (c) and SWI (d) with thrombus of varying ages in the periphery. MR Angiogram (e) Dilated feeding vessels (arrowhead) entering the aneurysmal malformation
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| Capillary Telangiectasia | | |
Capillary telangiectasias are clusters of dilated capillary-like vessels interspersed with the normal brain. These lesions account for 4-12 percent of vascular malformations and are often tiny, asymptomatic, and incidental observations, while symptoms such as bleeding, seizure, vertigo, tinnitus, and cranial nerve dysfunction have been reported in rare cases.[45] They are thought to be acquired lesions caused by underlying venous abnormalities. The majority are found in the pons, although they can also be found in the temporal lobe, medulla, or caudate. They are normally little, but in a few cases, they can grow to be larger than one cm. The majority are single lesions, however, in disorders such Osler-Weber Rendu, ataxia telangiectasia, and Sturge Weber, they can be numerous. On microscopic examination, there is no calcification, gliosis, or hemosiderin-laden macrophages in the neighboring brain, unlike other vascular malformations of the brain.[46]
IMAGING:
MRI
T2* (GRE, SWI) is the best sequence for demonstrating a BCT, visible as an area of poorly delineated grayish hypointensity.
BCTs typically show faint stippled or poorly delineated brush-like enhancement on T1 C+.[47]
Case 10: Case of a 13 year old male; T1(a); T2 (b) MR Angiography (c & d); MIP images of MR Angiography (e); Post-contrast Angiography images (f & g).
An abnormal tangle of arterial and venous flow voids/Serpiginous vessels seen in right temporal lobe with nidus (15.4 x 8.4 mm) supplied by right MCA and right anterior choroidal artery branches and drains into a right internal cerebral vein to the vein of Galen. Multiple small size venous channels and smaller capillaries are seen around the lesion in post contrast study – Suggestive of a combination of developmental venous anomalies and capillary Telangiectasis (Medusa head appearance).No e/o intranidal aneurysm, gliosis, or areas of ischemia were noted [Figure 10]. | Figure 10: Case 10: T1 (a) T2 (b) MR Angiography (c and d); MIP images MR Angiography (e); Post-contrast Angiography images (f and g): Abnormal tangle of arterial and venous serpiginous flow voids in right temporal lobe with nidus supplied by right MCA and anterior choroidal artery branches draining into a right internal cerebral vein to the vein of Galen. Multiple small-size venous channels and smaller capillaries are seen around the lesion in post contrast study
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| Discussion | | |
CNS vascular abnormalities come in a wide range of forms. Some of these lesions are aggressive, high-flow lesions that might cause hemorrhage or other complications, while others are more innocuous. Knowing the imaging characteristics of these lesions, and the findings that may indicate which ones are likely to hemorrhage or have other negative consequences, might help with treatment options.[48],[49],[50],[51],[52],[53]
[Table 8]. Imaging Characteristics Linked to Future Hemorrhage and Non-Hemorrhagic Neurologic Deficit.[50] | Table 8: Imaging characteristics linked to future hemorrhage and non-hemorrhagic neurologic deficit[28]
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The following conditions can have symptoms that are equivalent to vascular malformations of the brain. For a differential diagnosis, comparisons may be relevant.
Moyamoya disease
Moyamoya disease (Japanese for "puff of smoke") is a rare occlusive condition of unknown origin that primarily affects the supraclinoid segment of internal carotid arteries in the early stages, sparing the posterior fossa. Extensive minuscule basal perforator collateral arteries (the moyamoya vessels), which have been described as having a puff of smoke look on cerebral angiography, and transdural collateral vessels are generally developed. May present as hemorrhage, seizures, headaches, vision difficulties, and mental and psychiatric problems.[50]
Cerebral aneurysm
There is dilatation, bulging, or ballooning of part of the wall of a vein or artery. Cerebral aneurysms can happen at any age, but they are more common in adults than in children, and they affect women slightly more than men. The size and rate of growth of an unruptured cerebral aneurysm will influence the indications and symptoms. A small, unchanging aneurysm, for example, will usually cause no symptoms, whereas a larger aneurysm that is slowly expanding may cause symptoms such as facial numbness or vision issues. An individual may suffer symptoms such as a sudden and extremely strong headache, nausea, vision impairment, vomiting, and loss of consciousness just before an aneurysm ruptures.
Cerebrovascular accident (stroke)
Strokes happen when the blood flow to the brain is cut off or reduced. A thrombus narrows or totally closes an artery in the neck or head, resulting in a thrombotic stroke. The deposition of fat-containing compounds and calcium (plaque) on the inner linings of the blood vessels causes this (atherosclerosis or hardening of the arteries). When a clot breaks free from a diseased artery from another region of the body or the heart and blocks a smaller artery in the brain, it is known as an embolic stroke. Hemorrhagic strokes occur when a vessel in or around the brain ruptures, cutting off blood flow to that area. The symptoms, development, and prognosis of each form of stroke are unique. Clumsiness, headaches, speech problems, and weakness or paralysis on one or both sides of the body are all possible adverse effects. Symptoms include a stiff neck, nausea, vomiting, and loss of consciousness.
Abbreviations used in this article
PCA - Posterior cerebral artery
ICA - Internal carotid artery
SOV - Superior ophthalmic vein
DVA - Developmental venous anomaly
AVM - Arteriovenous malformation
MCA - Middle cerebral artery
ECA - External carotid artery
CS - Cavernous sinus
CM - Cavernous malformation
VOGM - Vein of galen malformation
| Conclusion | | |
The characteristic imaging findings of brain AVMs, and vascular brain lesions that can mimic brain AVMs, have been documented. Because these mimics have different natural histories and treatment options, it's critical for the radiologist to be able to tell them apart from a conventional brain AVM.
| Teaching Point | | |
Learning vascular malformations of the brain present to the doctors and identifying the imaging characteristics that help differentiate and categorize them and also know how to rule out their mimics.
Financial support and sponsorship
None.
Conflicts of interest
There are no conflicts of interest.
Bokhari MR, Bokhari SRA. Arteriovenous Malformation Of The Brain. 2022. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022. PMID: 28613495.
Claro E, Dias A, Girithari G, Massano A, Duarte MA. Non-traumatic hematomyelia: A rare finding in clinical practice. Eur J Case Rep Intern Med 2018;5:000961. doi: 10.12890/2018_000961.
Wu EM, El Ahmadieh TY, McDougall CM, Aoun SG, Mehta N, Neeley OJ, et al. Embolization of brain arteriovenous malformations with intent to cure: A systematic review. J Neurosurg 2019;132:388-399.
Xu H, Wang L, Guan S, Li D, Quan T. Embolization of brain arteriovenous malformations with the diluted Onyx technique: Initial experience. Neuroradiology 2019;61:471-8.
Heit JJ, Thakur NH, Iv M, Fischbein NJ, Wintermark M, Dodd RL, et al. Arterial-spin labeling MRI identifies residual cerebral arteriovenous malformation following stereotactic radiosurgery treatment. J Neuroradiol 2020;47:13-9.
Li W, Sun Q, Duan X, Yi F, Zhou Y, Hu Y, et al. [Etiologies and risk factors for young people with intracerebral hemorrhage]. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2018;43:1246-50.
Caranfa JT, Baldwin MT, Rutter CE, Bulsara KR. Synchronous cerebral arteriovenous malformation and lung adenocarcinoma carcinoma brain metastases: A case study and literature review. Neurochirurgie 2019;65:36-39.
Khandelwal A, Chaturvedi A, Singh GP, Mishra RK. Intractable brain swelling during cerebral arteriovenous malformation surgery due to contralateral acute subdural haematoma. Indian J Anaesth 2018;62:984-7.
Hofman M, Jamróz T, Kołodziej I, Jaskólski J, Ignatowicz A, Jakutowicz I, et al. Cerebral arteriovenous malformations-usability of Spetzler-Martin and Spetzler-Ponce scales in qualification to endovascular embolisation and neurosurgical procedure. Pol J Radiol 2018;83:e243-7.
D'Souza D, Mistry M, Gaillard F. Cerebrovascular malformations. https://doi.org/10.53347/rID-1084. [Last accessed on 2022 Aug 20].
Berenstein A, Lasjaunias P, terBrugge KG. Surgical Neuroangiography. 2.1. Clinical and Endovascular Treatment Aspects in Adults. 2nd ed. Berlin: Springer; 2004.
Friedlander RM. Clinical practice: Arteriovenous malformations of the brain. N Engl J Med 2007;356:2704-12.
Hoh BL, Putman CM, Budzik RF, Ogilvy CS. Surgical and endovascular flow disconnection of intracranial pial single-channel arteriovenous fistulae. Neurosurgery 2001;49:1351-63; discussion 1363-4.
Kakino S, Ogasawara K, Kubo Y, Ogawa A. Spontaneous pial single-channel arteriovenous fistulae with angiographically occult small feeding arteries: Case report. Surg Neurol 2008;69:187-90; discussion 191.
Weon YC, Yoshida Y, Sachet M, Mahadevan J, Alvarez H, Rodesch G, et al. Supratentorial cerebral arteriovenous fistulas (AVFs) in children: Review of 41 cases with 63 non choroidal single-hole AVFs. Acta Neurochir (Wien) 2005;147:17-31; discussion 31.
Choi JH, Mohr JP. Brain arteriovenous malformations in adults. Lancet Neurol 2005;4:299-308.
Söderman M, Andersson T, Karlsson B, Wallace MC, Edner G. Management of patients with brain arteriovenous malformations. Eur J Radiol 2003;46:195-205.
Copelan AZ, Krishnan A, Marin H, Silbergleit R. Dural arteriovenous fistulas: A characteristic pattern of edema and enhancement of the medulla on MRI. Am J Neuroradiol 2018;39238-44.
Kwon BJ, Han MH, Kang HS, Chang KH. MR imaging findings of intracranial dural arteriovenous fistulas: Relations with venous drainage patterns. AJNR Am J Neuroradiol 2005;26:2500-7.
Gaensler EH, Jackson DE Jr, Halbach VV. Arteriovenous fistulas of the cervicomedullary junction as a cause of myelopathy: Radiographic findings in two cases. AJNR Am J Neuroradiol 1990;11:518-21.
Hähnel S, Jansen O, Geletneky K. MR appearance of an intracranial dural arteriovenous fistula leading to cervical myelopathy. Neurology 1998;51:1131-35.
Li J, Ezura M, Takahashi A, Yoshimoto T. Intracranial dural arteriovenous fistula with venous reflux to the brainstem and spinal cord mimicking brainstem infarction: Case report. Neurol Med Chir (Tokyo) 2004;44:24-8.
Cahan LD, Higashida RT, Halbach VV, Hieshima GB. Variants of radiculomeningeal vascular malformations of the spine. J Neurosurg 1987;66:333-7.
Hassler W, Thron A. Flow velocity and pressure measurements in spinal dural arteriovenous fistulas. Neurosurg Rev 1994;17:29-36
Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 1969;93:1071-8.
Kohli GS, Patel BC. Carotid cavernous fistula. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2022. Available from: https://www.ncbi.nlm.nih.gov/books/NBK535409/. [Last accessed on 2022 May 24].
Ellis JA, Goldstein H, Connolly ES, Meyers PM. Carotid-cavernous fistulas. Neurosurg Focus 2012;32:E9.
Barrow DL, Spector RH, Braun IF, Landman JA, Tindall SC, Tindall GT. Classification and treatment of spontaneous carotid-cavernous sinus fistulas. J Neurosurg 1985;62:248-56.
Henderson AD, Miller NR. Carotid-cavernous fistula: Current concepts in aetiology, investigation, and management. Eye (Lond) 2018;32:164-72.]
Rammos SK, Maina R, Lanzino G. Developmental venous anomalies: Current concepts and implications for management. Neurosurgery 2009;65:20-9; discussion 29-30.
Willinsky R, Terbrugge K, Montanera W, Mikulis D, Wallace MC. Venous congestion: An MR finding in dural arteriovenous malformations with cortical venous drainage. AJNR Am J Neuroradiology 1994;15: 1501-7.
Söderman M, Pavic L, Edner G, Holmin S, Andersson T. Natural history of dural arteriovenous shunts. Stroke 2008;39:1735-1739.
van Dijk JM, terBrugge KG, Willinsky RA, Wallace MC. Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke 2002;33:1233-6.
D'Souza D, Mistry M, Gaillard F. Cerebrovascular malformations. https://doi.org/10.53347/rID-1084. [Last accessed on 2022 Aug 20].
Caton MT, Shenoy VS. Cerebral cavernous malformations. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022. Available from: https://www.ncbi.nlm.nih.gov/books
/NBK538144/. [Last accessed on 2022 Apr 19].
Padarti A, Zhang J. Recent advances in cerebral cavernous malformation research. Vessel Plus 2018;2:21. doi: 10.20517/2574-1209.2018.34.
Sarwar M, McCormick WF. Intracerebral venous angioma. Case report and review. Arch Neurol 1978;35:323-5.
Uchino A, Hasuo K, Matsumoto S. Double cerebral venous angiomas: MRI. Neuroradiology 1995:37;25-8. https://doi.org/10.1007/BF00588514. [Last accessed on 2022 Aug 20].
Huber G, Henkes H, Hermes M, Felber S, Terstegge K. Regional association of developmental venous anomalies with angiographically occult vascular malformations. Eur Radiol 1996;6:30-7.
San Millan Ruiz D, Delavelle J, Yilmaz H, Gailloud P, Piovan E, Bertramello A, et al. Parenchymal abnormalities associated with developmental venous anomalies. Neuroradiology 2007;49:987-95.
Brevis Nuñez F, Dohna-Schwake C. Epidemiology, diagnostics, and management of vein of Galen malformation. Pediatr Neurol 2021;119:50-5.
Vascular Malformations of the Brain: Radiologic and Pathologic Correlation. Alice Boyd Smith, Lt. Col. USAF MC. J Am Osteopath Coll Radiol 2012;1.
Moriarity JL, Clatterbuck RE, Rigamonti D. The natural history of cavernous malformations. Neurosurg Clin N Am 1999;10:411M7.
Batra S, Lin D, Recinos PF, Zhang J, Rigamonti D. Cavernous malformations: Natural history, diagnosis and treatment. Nat Rev Neurol 2009;5:659-70.
Li DY, Whitehead KJ. Evaluating strategies for the treatment of cerebral cavernous malformations. Stroke 2010;41 (10 Suppl):p.S92-4.
Raybaud CA, Strother CM, Hald JK. Aneurysms of the vein of Galen: Embryonic considerations and anatomical features relating to the pathogenesis of the malformation. Neuroradiology 1989;31:109-28.
Weerakkody Y, El-Feky M. CNS capillary telangiectasia. Reference article, Radiopaedia.org. https://doi.org/10.53347
/rID-7725. [Last accessed on 2020 Oct 02].
Hoang S, Choudhri O, Edwards M, Guzman R. Vein of Galen malformation. Neurosurg Focus 2009;27:E8.
Gharavi SM, Tang Y. Cerebral Vascular Malformations. In: Atlas More Details of Emergency Neurovascular Imaging. Springer, Cham. 2020. https://doi.org/10.1007/978-3-030-43654-4_9. [Last accessed on 2022 Aug 20].
Gatscher S, Brew S, Banks T, Simcock C, Sullivan Y, Crockett J. Multislice spiral computed tomography for pediatric intracranial vascular pathophysiologies. J Neurosurg 2007;107 (3 Suppl):203-8.
Sayama CM, Osborn AG, Chin SS, Couldwell WT. Capillary telangiectasias: Clinical, radiographic, and histopathological features. Clinical article. J Neurosurg 2010;113:709-14.
McCormick PW, Spetzler RF, Johnson PC, Drayer BP. Cerebellar hemorrhage associated with capillary telangiectasia and venous angioma: A case report. Surg Neurol 1993;39:451-7.
Geibprasert S, Pongpech S, Jiarakongmun P, Shroff MM, Armstrong DC, Krings T. Radiologic assessment of brain arteriovenous malformations: What clinicians need to know. Radiographics 2010;30:483-501.
MJDRDYPU_756_22F1
Figure
Figure 1: Case 1: (a) T2 (b) FLAIR sequences showing flow voids (arrow) on in the left parieto-occipital region with dilated cortical veins along cortex. Nidus is seen containing gliotic brain parenchyma. (c) Blooming in vascular channels on GRE (arrow). (d and e) MR Angio sequence and (f) Contrast Venous sequence show AVM (arrow) in the left occipito-parietal lobe. (f) Contrast Venous sequence shows a nidus in the parieto-occipital region (arrow) with shunting between the branches of PCA and the cortical veins
[Figure 1]
MJDRDYPU_756_22F2
Figure
Figure 2: Case 2: T2 (a) FLAIR (b) sequences show flow voids (arrow) in the right frontal lobe with nidus. (c) GRE sequences show blooming (arrow). (d) MR Angio sequence show branches of MCA (arrow) seen communicating with the nidus. (e) Contrast Venous sequence shows a nidus in the frontal region with shunting between the branches of MCA and the cortical veins (arrow)
[Figure 2]
MJDRDYPU_756_22F3
Figure
Figure 3: Case 3: (a) and (b) Multiple flow voids (arrow) noted on T2 and FLAIR sequences in the right parietal region with dilated cortical veins along the cortex. Nidus is seen containing gliotic brain parenchyma. (c) Blooming (arrow) on gradient images. (d) MR Angio sequence show branches of MCA seen communicating with the nidus and early draining cortical veins (arrow). (e) Contrast Venous sequence shows a nidus in the parietal region with shunting between the branches of MCA and the cortical veins (arrow)
[Figure 3]
MJDRDYPU_756_22F4
Figure
Figure 4: Case 4: (a) and (b) T2 and FLAIR sequences show an area of altered signal intensity (arrow) noted in the left occipital lobe with multiple flow voids. Numerous extensive prominent and tortuous dural varicosities (arrowhead) were noted predominantly near the left transverse sinuses. (c) Blooming (arrow) on gradient images. (d) MR Venogram sequence shows Numerous and extensive prominent and tortuous dural varicosities (arrow) noted predominantly near left transverse sinuses
[Figure 4]
MJDRDYPU_756_22F5
Figure
Figure 5: Case 5: (a) Dilated left half of the cavernous sinus with T2 flow void within (arrow) and (b) Asymmetrically dilated and tortuous left superior ophthalmic vein (arrow). (c) Large partly thrombosed aneurysm noted in the cavernous segment of left ICA (arrow) bulging along medial and lateral margin of the left cavernous sinus. High flow communication between the intracavernous portion of the left ICA and the left cavernous sinus was also noted
[Figure 5]
MJDRDYPU_756_22F6
Figure
Figure 6: Case 6: T1C+ (d) Enlarged medullary veins (arrow) are seen in the right gangliocapsular area with a characteristic "Medusa head" appearance draining into a single larger collecting vein (arrowhead) which is directed inferno-medially towards the body of right lateral ventricle to drain into a deep ependymal vein. The above-mentioned collecting vein appears show a flow void (arrow) on T1 sequence (a) T2/FLAIR hyperintensity suggestive of partial gliosis (arrow) (b and amp; c)
[Figure 6]
MJDRDYPU_756_22F7
Figure
Figure 7: Case 7: Altered signal intensity area (arrow) appearing isointense on T1W (a), hyperintense on T2W/FLAIR (b), with no diffusion restriction and blooming (arrow) on SWI sequence (c). T1 contrast-venous study (d-f) shows subtle enhancement with medusa head appearance (arrow) of prominent medullary veins (arrow) converging in transcortical collector vein (arrow)
[Figure 7]
MJDRDYPU_756_22F8
Figure
Figure 8: Case 8: Area of altered signal intensity (arrows) appearing heterogeneously hyperintense on T1W (a) hypointense on T2WI/FLAIR (b and c), showing blooming on gradient images, hemo (d) and SWI (e) with corresponding hyperintensity on PHASE (f) in right precentral gyrus with fluid-fluid level and hypointense rim
[Figure 8]
MJDRDYPU_756_22F9
Figure
Figure 9: Case 9: Marked aneurysmal dilatation of vein of galen (arrow) exhibiting hypointensity on T2W (b) and T1W (a). Dilated bilateral posterior cerebral artery branches, internal cerebral vein, falcine sinus, straight sinus, bilateral transverse, and sigmoid sinuses. Acute obstructive hydrocephalus. Signal misinterpretation (arrow) on Phase (c) and SWI (d) with thrombus of varying ages in the periphery. MR Angiogram (e) Dilated feeding vessels (arrowhead) entering the aneurysmal malformation
[Figure 9]
MJDRDYPU_756_22F10
Figure
Figure 10: Case 10: T1 (a) T2 (b) MR Angiography (c and d); MIP images MR Angiography (e); Post-contrast Angiography images (f and g): Abnormal tangle of arterial and venous serpiginous flow voids in right temporal lobe with nidus supplied by right MCA and anterior choroidal artery branches draining into a right internal cerebral vein to the vein of Galen. Multiple small-size venous channels and smaller capillaries are seen around the lesion in post contrast study
[Figure 10]
MJDRDYPU_756_22T1
Table
Table 1: High or low flow cerebral vascular malformations[1]
[Table 1]
MJDRDYPU_756_22T2
Table
Table 2: Functional classification: With or without AV shunting[1]
[Table 2]
MJDRDYPU_756_22T3
Table
Table 3: Spetzler-Martin arteriovenous malformation (AVM) grading system
[Table 3]
MJDRDYPU_756_22T4
Table
Table 4: Can be of two types: Direct or indirect
[Table 4]
MJDRDYPU_756_22T5
Table
Table 5: Classified into four types (Barrow classification)
[Table 5]
MJDRDYPU_756_22T6
Table
Table 6: Angiography findings
[Table 6]
MJDRDYPU_756_22T7
Table
Table 7: The Zabramski classification of cerebral cavernomas
[Table 7]
MJDRDYPU_756_22T8
Table
Table 8: Imaging characteristics linked to future hemorrhage and non-hemorrhagic neurologic deficit[28]
[Table 8]
| References | | |
| 1. | Bokhari MR, Bokhari SRA. Arteriovenous Malformation Of The Brain. 2022. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022. PMID: 28613495.  |
| 2. | Claro E, Dias A, Girithari G, Massano A, Duarte MA. Non-traumatic hematomyelia: A rare finding in clinical practice. Eur J Case Rep Intern Med 2018;5:000961. doi: 10.12890/2018_000961. |
| 3. | Wu EM, El Ahmadieh TY, McDougall CM, Aoun SG, Mehta N, Neeley OJ, et al. Embolization of brain arteriovenous malformations with intent to cure: A systematic review. J Neurosurg 2019;132:388-399. |
| 4. | Xu H, Wang L, Guan S, Li D, Quan T. Embolization of brain arteriovenous malformations with the diluted Onyx technique: Initial experience. Neuroradiology 2019;61:471-8. |
| 5. | Heit JJ, Thakur NH, Iv M, Fischbein NJ, Wintermark M, Dodd RL, et al. Arterial-spin labeling MRI identifies residual cerebral arteriovenous malformation following stereotactic radiosurgery treatment. J Neuroradiol 2020;47:13-9. |
| 6. | Li W, Sun Q, Duan X, Yi F, Zhou Y, Hu Y, et al. [Etiologies and risk factors for young people with intracerebral hemorrhage]. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2018;43:1246-50. |
| 7. | Caranfa JT, Baldwin MT, Rutter CE, Bulsara KR. Synchronous cerebral arteriovenous malformation and lung adenocarcinoma carcinoma brain metastases: A case study and literature review. Neurochirurgie 2019;65:36-39. |
| 8. | Khandelwal A, Chaturvedi A, Singh GP, Mishra RK. Intractable brain swelling during cerebral arteriovenous malformation surgery due to contralateral acute subdural haematoma. Indian J Anaesth 2018;62:984-7. [Full text] |
| 9. | Hofman M, Jamróz T, Kołodziej I, Jaskólski J, Ignatowicz A, Jakutowicz I, et al. Cerebral arteriovenous malformations-usability of Spetzler-Martin and Spetzler-Ponce scales in qualification to endovascular embolisation and neurosurgical procedure. Pol J Radiol 2018;83:e243-7. |
| 10. | |
| 11. | Berenstein A, Lasjaunias P, terBrugge KG. Surgical Neuroangiography. 2.1. Clinical and Endovascular Treatment Aspects in Adults. 2 nd ed. Berlin: Springer; 2004. |
| 12. | Friedlander RM. Clinical practice: Arteriovenous malformations of the brain. N Engl J Med 2007;356:2704-12. |
| 13. | Hoh BL, Putman CM, Budzik RF, Ogilvy CS. Surgical and endovascular flow disconnection of intracranial pial single-channel arteriovenous fistulae. Neurosurgery 2001;49:1351-63; discussion 1363-4. |
| 14. | Kakino S, Ogasawara K, Kubo Y, Ogawa A. Spontaneous pial single-channel arteriovenous fistulae with angiographically occult small feeding arteries: Case report. Surg Neurol 2008;69:187-90; discussion 191. |
| 15. | Weon YC, Yoshida Y, Sachet M, Mahadevan J, Alvarez H, Rodesch G, et al. Supratentorial cerebral arteriovenous fistulas (AVFs) in children: Review of 41 cases with 63 non choroidal single-hole AVFs. Acta Neurochir (Wien) 2005;147:17-31; discussion 31. |
| 16. | Choi JH, Mohr JP. Brain arteriovenous malformations in adults. Lancet Neurol 2005;4:299-308. |
| 17. | Söderman M, Andersson T, Karlsson B, Wallace MC, Edner G. Management of patients with brain arteriovenous malformations. Eur J Radiol 2003;46:195-205. |
| 18. | Copelan AZ, Krishnan A, Marin H, Silbergleit R. Dural arteriovenous fistulas: A characteristic pattern of edema and enhancement of the medulla on MRI. Am J Neuroradiol 2018;39238-44. |
| 19. | Kwon BJ, Han MH, Kang HS, Chang KH. MR imaging findings of intracranial dural arteriovenous fistulas: Relations with venous drainage patterns. AJNR Am J Neuroradiol 2005;26:2500-7. |
| 20. | Gaensler EH, Jackson DE Jr, Halbach VV. Arteriovenous fistulas of the cervicomedullary junction as a cause of myelopathy: Radiographic findings in two cases. AJNR Am J Neuroradiol 1990;11:518-21. |
| 21. | Hähnel S, Jansen O, Geletneky K. MR appearance of an intracranial dural arteriovenous fistula leading to cervical myelopathy. Neurology 1998;51:1131-35. |
| 22. | Li J, Ezura M, Takahashi A, Yoshimoto T. Intracranial dural arteriovenous fistula with venous reflux to the brainstem and spinal cord mimicking brainstem infarction: Case report. Neurol Med Chir (Tokyo) 2004;44:24-8. |
| 23. | Cahan LD, Higashida RT, Halbach VV, Hieshima GB. Variants of radiculomeningeal vascular malformations of the spine. J Neurosurg 1987;66:333-7. |
| 24. | Hassler W, Thron A. Flow velocity and pressure measurements in spinal dural arteriovenous fistulas. Neurosurg Rev 1994;17:29-36 |
| 25. | Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 1969;93:1071-8. |
| 26. | |
| 27. | Ellis JA, Goldstein H, Connolly ES, Meyers PM. Carotid-cavernous fistulas. Neurosurg Focus 2012;32:E9. |
| 28. | Barrow DL, Spector RH, Braun IF, Landman JA, Tindall SC, Tindall GT. Classification and treatment of spontaneous carotid-cavernous sinus fistulas. J Neurosurg 1985;62:248-56. |
| 29. | Henderson AD, Miller NR. Carotid-cavernous fistula: Current concepts in aetiology, investigation, and management. Eye (Lond) 2018;32:164-72.] |
| 30. | Rammos SK, Maina R, Lanzino G. Developmental venous anomalies: Current concepts and implications for management. Neurosurgery 2009;65:20-9; discussion 29-30. |
| 31. | Willinsky R, Terbrugge K, Montanera W, Mikulis D, Wallace MC. Venous congestion: An MR finding in dural arteriovenous malformations with cortical venous drainage. AJNR Am J Neuroradiology 1994;15: 1501-7. |
| 32. | Söderman M, Pavic L, Edner G, Holmin S, Andersson T. Natural history of dural arteriovenous shunts. Stroke 2008;39:1735-1739. |
| 33. | van Dijk JM, terBrugge KG, Willinsky RA, Wallace MC. Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke 2002;33:1233-6. |
| 34. | |
| 35. | Caton MT, Shenoy VS. Cerebral cavernous malformations. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2022. Available from: https://www.ncbi.nlm.nih.gov/books/NBK538144/. [Last accessed on 2022 Apr 19]. |
| 36. | Padarti A, Zhang J. Recent advances in cerebral cavernous malformation research. Vessel Plus 2018;2:21. doi: 10.20517/2574-1209.2018.34. |
| 37. | Sarwar M, McCormick WF. Intracerebral venous angioma. Case report and review. Arch Neurol 1978;35:323-5. |
| 38. | |
| 39. | Huber G, Henkes H, Hermes M, Felber S, Terstegge K. Regional association of developmental venous anomalies with angiographically occult vascular malformations. Eur Radiol 1996;6:30-7. |
| 40. | San Millan Ruiz D, Delavelle J, Yilmaz H, Gailloud P, Piovan E, Bertramello A, et al. Parenchymal abnormalities associated with developmental venous anomalies. Neuroradiology 2007;49:987-95. |
| 41. | Brevis Nuñez F, Dohna-Schwake C. Epidemiology, diagnostics, and management of vein of Galen malformation. Pediatr Neurol 2021;119:50-5. |
| 42. | Vascular Malformations of the Brain: Radiologic and Pathologic Correlation. Alice Boyd Smith, Lt. Col. USAF MC. J Am Osteopath Coll Radiol 2012;1. |
| 43. | Moriarity JL, Clatterbuck RE, Rigamonti D. The natural history of cavernous malformations. Neurosurg Clin N Am 1999;10:411M7. |
| 44. | Batra S, Lin D, Recinos PF, Zhang J, Rigamonti D. Cavernous malformations: Natural history, diagnosis and treatment. Nat Rev Neurol 2009;5:659-70. |
| 45. | Li DY, Whitehead KJ. Evaluating strategies for the treatment of cerebral cavernous malformations. Stroke 2010;41 (10 Suppl):p.S92-4. |
| 46. | Raybaud CA, Strother CM, Hald JK. Aneurysms of the vein of Galen: Embryonic considerations and anatomical features relating to the pathogenesis of the malformation. Neuroradiology 1989;31:109-28. |
| 47. | Weerakkody Y, El-Feky M. CNS capillary telangiectasia. Reference article, Radiopaedia.org. https://doi.org/10.53347/rID-7725. [Last accessed on 2020 Oct 02]. |
| 48. | Hoang S, Choudhri O, Edwards M, Guzman R. Vein of Galen malformation. Neurosurg Focus 2009;27:E8. |
| 49. | |
| 50. | Gatscher S, Brew S, Banks T, Simcock C, Sullivan Y, Crockett J. Multislice spiral computed tomography for pediatric intracranial vascular pathophysiologies. J Neurosurg 2007;107 (3 Suppl):203-8. |
| 51. | Sayama CM, Osborn AG, Chin SS, Couldwell WT. Capillary telangiectasias: Clinical, radiographic, and histopathological features. Clinical article. J Neurosurg 2010;113:709-14. |
| 52. | McCormick PW, Spetzler RF, Johnson PC, Drayer BP. Cerebellar hemorrhage associated with capillary telangiectasia and venous angioma: A case report. Surg Neurol 1993;39:451-7. |
| 53. | Geibprasert S, Pongpech S, Jiarakongmun P, Shroff MM, Armstrong DC, Krings T. Radiologic assessment of brain arteriovenous malformations: What clinicians need to know. Radiographics 2010;30:483-501. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8]
|
