Chapter 13 Vascular Anomalies of the Brain
INTRODUCTION TO ANGIOGRAPHIC MODALITIES
Catheter Angiography
Cerebral angiography was one of the first diagnostic modalities for brain diseases, and it has remained crucially important and routinely used since its description by Egaz Moniz in 1927.1 However, there has been significant evolution from the direct carotid cut downs and cut film technique of the 1920s to digital subtraction angiography with three-dimensional (3D) reconstruction.
With the transition to non-ionic contrast, smaller 4- and 5-French, and more flexible catheters and guidewires with hydrophilic coating, the risk for permanent neurologic injury was reduced from 1% to 2.4%2,3 to less than 0.1% to 0.3%.4–6 However, given risk of local pain, bruising, and hematoma in up to 25% of cases, noninvasive alternatives should be considered whenever they will provide similar diagnostic information.
Cerebral angiography remains the gold standard in the diagnosis of dural arteriovenous fistulas (dAVFs), as well as small aneurysms and arteriovenous malformations (AVMs). In addition, super-selective angiography can provide functional and physiological data important for clinical decision analysis, although pressure measurements are not commonly performed. It is still strongly recommended that a magnetic resonance imaging (MRI) study and a four-vessel angiogram be obtained to delineate the anatomy of an AVM.7 Computed tomography (CT) angiography can outline enlarged abnormal cortical veins but may miss subtle dural venous drainage or small arteriovenous malformations.8 MRI may show important indirect signs such as edema and abnormal cortical enhancement. In our practice, all patients with unexplained subarachnoid, subdural, or atypical parenchymal hemorrhage undergo digital subtraction angiography (DSA).
Three-Dimensional Digital Subtraction Angiography
Excellent spatial resolution and lack of artifact has made 3D DSA an attractive tool for treatment planning and follow-up (Figure 13-1). It further increases the sensitivity for detection of aneurysms smaller than 3 mm9 and provides invaluable conformational information for endovascular treatment planning (Figure 13-2).
Computed Tomography Angiography
Multidetector CT angiography (MDCTA) has higher spatial resolution and decreased, but not eliminated, propensity to motion artifacts (Figure 13-33) than MRA.10,11 For these reasons, MDCTA has largely replaced MR angiography in our practice.
Figure 13-33 Computed tomography (CT) angiography with motion artifact. The CT angiogram suggested moderate perianeurysmal vasospasm, which was not confirmed by digital substraction angiography (see Figure 13-34 A and B,).
The sensitivity for detection of even small aneurysms has substantially increased. One study found MDCTA to be actually more sensitive than DSA for the detection of small aneurysms.12 Yet DSA remains the gold standard for aneurysm detection. Colen et al.13 found that during screening of patients with nontraumatic subarachnoid hemorrhage, MDCTA missed the primary aneurysm in 11 of 211 cases. Regions with overprojecting bone (such as the cavernous segment or supraclinoid carotid artery) may not be optimally visualized,14,15 and MDCTA has lower sensitivity in detecting branches incorporated into the aneurysmal sac.16
The bony structures of the sella are often manually excluded on the reconstruction and thus an aneurysm can easily be “removed” in the cavernous and supraclinoid region (as seen in Figure 13-31, F). Careful analysis of the source images is crucial to preserve high sensitivity. Inadequate bolus timing with poor arterial and dense venous filling can render interpretation of CT angiography much more challenging. Still, CT angiography can be superior to DSA for aneurysms with competing flow, such as some basilar tip, basilar trunk, or anterior communicating aneurysms because it avoids the problem of contrast “washout” (see Figure 13-18).
CT angiography is valuable for follow-up of aneurysms treated with titanium alloy clips, but it is not useful when cobalt alloy clips have been used.17 Image quality is also degraded by orientation of the clip perpendicular to the imaging axis or presence of multiple clips. Streak artifacts caused by platinum coils make it an unsuitable method to assess for recanalization of embolized aneurysms. (See Figures 13-3 and 13-4.)
In our institution, patients with subarachnoid or atypical intracranial hemorrhage are generally screened with CT angiography. An aneurysmal source of bleeding can often be identified in the emergency room, allowing triage to endovascular versus surgical treatment.
If the CT angiography is nondiagnostic, DSA is always performed to evaluate for a missed aneurysm or nonaneurysmal sources, such as a dural arteriovenous (AV) fistula. See Figure 13-5.
However, protocols relying directly on DSA are also very acceptable and may actually reduce cost.
Magnetic Resonance Angiography
TOF techniques exploit the contrast between the high signal intensity of inflowing, fully magnetized blood and the low signal intensity of saturated stationary tissue. Multiple thin imaging slices (two-dimensional [2D]) or larger slabs (3D) perpendicular to the axis of flow are acquired with a flow-compensated gradient-echo sequence. Three-dimensional TOF angiography allows greater spatial resolution and is more resistant to signal loss from disturbed flow than 2D TOF. However, PC MRA and TOF MRA are sensitive to artifacts caused by turbulent or slow flow (Figure 13-6, B). TOF is also affected by in-plane artifacts.
Contrast-enhanced (TOF) MR angiography has been employed to overcome these problems. It is performed by intravenously injecting a contrast agent to shorten selectively the T1 of the blood to produce the signal, rather than relying on flow. By implementing a T1-weighted imaging sequence during the first pass of the contrast agent, images can be produced showing arteries in striking contrast relative to surrounding stationary tissues and veins. However, synchronizing the acquisition with the arrival of the contrast agent is critical to ensure image quality. For a more detailed discussion on these MR angiography techniques, the reader is referred to the review authored by Aygun.18
Whereas MRA for follow-up of clipped aneurysms is limited by severe “blooming” artifact, it is usually adequate to monitor coiled aneurysms because it has a sensitivity of 75% for detecting a residual neck.19 See Figure 13-7. However, problems related to signal drop-out may occur (Figure 13-8).
No clear information has emerged on whether contrast-enhanced MR angiography is superior to conventional 3D TOF.19,20 Where available, contrast-enhanced 3-Tesla MRA may a superior diagnostic option.21
DSA remains the gold standard for the detection of small AV malformations and dural AV fistulas. Although specialized sequences such as 3T four-dimensional MRA22 and others23 show good correlation for size of feeders and AVM classification, DSA is still more reliable in the diagnosis of small AVMs, which can be missed even by repeated MRA studies.24 Contrast-enhanced MRA can be used to follow dural AV fistulas, but it is less sensitive than DSA (Figure 13-9).25
COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE IMAGING
CT without contrast is poorly sensitive for brain aneurysms. However, unruptured aneurysms may present with rim calcification or slight hyperdensity due to the blood contained in the aneurysm. Only relatively large (≥10mm) aneurysms can be seen on plain CT scan, however (Figure 13-10).
CT without contrast is the standard screening test when subarachnoid hemorrhage is suspected (see Chapter 12), but almost all aneurysm locations in the circle of Willis can produce diffuse and symmetric subarachnoid hemorrhage and a dedicated vascular study is necessary to define the source of bleeding. Sometimes an aneurysm can be seen as a hypodense region within dense subarachnoid hemorrhage, a finding often referred to as a “ghost sign.” The distribution of the blood can be helpful to predict the location of the ruptured aneurysm, especially when multiple aneurysms are present at the time of hemorrhage. The location of parenchymal hemorrhage is typically adjacent to the point of rupture (Figure 13-11).
Unenhanced CT of the brain has poor sensitivity for vascular malformations but sometimes outlines enlarged draining veins of AVMs (Figure 13-12, A). Administration of contrast significantly increases the sensitivity of CT scans for the diagnosis of vascular abnormalities.
MRI
MRI of the brain, although more sensitive than CT, is not adequate to rule out the presence of an aneurysm. However, given the frequent use of this technique as screening test for many neurologic conditions, most of the incidental aneurysms treated in our institution are identified by this technique. Indirect markers are additional flow voids adjacent to vessels or, less commonly, perianeurysmal gliosis (see Figure 13-39 B,).
Rarely, slow flow within the aneurysm can cause high signal of fluid-attenuated inversion recovery (FLAIR)/T2, which can be confused with focal thrombus or hemorrhage (Figure 13-13).
MRI is indispensable in the diagnosis and management planning of AVMs and is part of the routine diagnostic workup preceding the treatment of these lesions (see Figures 13-12 B–C, and 13-43 A–C,).
ANEURYSMS
General Concepts
Types of Aneurysms
Nonsaccular Aneurysms
Fusiform Aneurysms
Transitional Forms
Dolichoectasia
Saccular Aneurysms
TREATMENT
In the past, surgical obliteration (“clipping”) was the main method of treatment of ruptured aneurysms. Since the introduction of detachable coils,50 there has been a progressive increase in the use of coil embolization for the treatment of both ruptured and unruptured aneurysms; nonetheless, the controversy about the optimal management of intracranial aneurysms is far from settled.
Despite various criticisms, the largest trial comparing clipping versus coiling of ruptured aneurysms, the International Subarachnoid Aneurysm Trial (ISAT), has provided Class I evidence indicating that endovascular therapy (EVT) results in superior 1-year outcomes compared with surgical repair of ruptured aneurysms equally amenable to both types of treatment (Figure 13-30).51
The risk of subarachnoid hemorrhage from unruptured intracranial aneurysms (UIA) as well as the risk of their treatment remains poorly defined. In the ISUIA, the largest study on the natural history of UIA, the cumulative 5-year rupture rates for untreated aneurysms in patients without previous aneurysmal SAH ranged from 0% to 40% in the anterior circulation, and 2.5% to 50% in the posterior circulation depending on aneurysm size26 (Table 13-1).
TABLE 13-1 Five-year cumulative rupture rates according to size and location of unruptured aneurysm.26
No randomized trial has compared elective aneurysm clipping versus coiling. A review of more than 2500 patients with UIA showed adverse outcomes were significantly more common in surgical cases (18.5%) compared with endovascular cases (10.6%) with an in-hospital mortality of 2.3% versus 0.4%.52
Incomplete occlusion of aneurysms is more common with endovascular therapy (Figure 13-31). Reported rates of initial complete occlusion of ruptured aneurysms treated with EVT are relatively low (40%–68%), and up to 34% require two or more procedures to achieve complete occlusion.46,53,54 However, progressive thrombosis or healing may contribute to occlude the aneurysm over time in approximately 20% of patients with initial remnants.55
Another major criticism of EVT is the possibility of recanalization (ranging from 15% to 30%), most frequently seen in wide-necked and large aneurysms (>10 mm).56,57 In one study, recanalization was not seen in aneurysms with “packing densities” greater than 24% and volumes less than 200 mm3. Aneurysms with volumes greater than 600 mm3 (equivalent to 10.4 mm spherical diameter) could not be densely packed and recanalized in nearly 90% of cases.58 “Bioactive coils” have not yet been shown to reduce the rate of recanalization and may even be detrimental.59,60 A recent study using a liquid embolic agent (Onyx) has shown promising results with no recanalization in aneurysms less than 10 mm and a low rate of recanalization (4%) for stent-assisted embolization of large and giant aneurysms.45
Aneurysm recanalization has been reported to be associated with a significant risk of hemorrhage (7.9% over 5 years).61
The risk of elective retreatment of recanalized aneurysms appears to be much lower than during the acute phase after SAH. Near-complete or complete occlusion can be achieved in more than three quarters of cases, with very low risk of procedural complications.62
Late rebleeding (> 1 month after embolization) occurred at a rate of 0.32% per year in a series of 393 ruptured aneurysms treated between 1995 and 2003 over a mean follow-up of 48 months.63 Rebleeding has been seen as late as 2010 days after treatment.64 If recanalization is detected and treated, the risk of late rerupture is low (0.11%/year).65,66 Follow-up imaging is thus required after aneurysm coiling. MRA may be equivalent to conventional angiography for this purpose.67
After aneurysm remnants are stable for more than 12 months, they are unlikely to rebleed.55,61,68
A 62-year-old woman with history of smoking, hypertension, and fibromyalgia presented with acute syncope and severe headache. In the emergency department, the patient was awake but confused (Hess and Hunt Grade III). CT scan of the brain showed an extensive SAH in the basal cisterns (Fisher Grade 3) with predominant extension into the left sylvian fissure. The upper portions of the interhemispheric fissure were largely spared (Figure 13-32 A–B,).
CT angiography (Figure 13-33) showed a 6-mm anterior communicating artery aneurysm. The visualization was limited by irregularities due to motion artifact on the reconstructed 3D images.
The patient underwent diagnostic catheter angiography with 3D DSA, and the broad-necked anterior communicating artery aneurysm was deemed amenable to coil embolization (Figure 13-34). An incidental 3-mm pericallosal aneurysm was seen, but given the lack of blood in the upper interhemispheric fissure, it was not considered to be the source of bleeding. This aneurysm had not been reported on the CT angiogram, but in retrospect, it was also visible on the reconstruction and, particularly, the source images of this study.
The patient underwent embolization of the anterior communicating artery aneurysm without complications (Figure 13-34 D,), followed in the same session by embolization of the right pericallosal aneurysm, which was primarily filled from the contralateral right carotid artery (Figure 13-35).
On the fourth day after SAH, transcranial Doppler (TCD) velocities in the left MCA were 62cm/sec with an ICA to MCA ratio of 2.3. On post-bleeding day 5 the patient became increasingly agitated, dysphasic and developed right hemiparesis. She was started on aggressive hemodynamic augmentation therapy. CT perfusion only showed subtle reduction and delay of cerebral blood flow in the left MCA territory (Figure 13-36).
Because of her acute neurological deficits, a diagnostic catheter angiography was performed showing moderately severe distal left MCA vasospasm. The patient was treated with intra-arterial nicardipine. She improved but continued to require very high doses of vasopressors. On Day 6, the patient became abruptly hemiplegic and globally aphasic. MRI showed only spotty areas of restricted diffusion and normal FLAIR signal, suggestive of salvageable left MCA territory (Figure 13-37).
The patient underwent emergent angiography, which revealed global vasospasm, most severe in the left A1 and M1 segments (Figure 13-38A,). Bilateral infusion of nicardipine and angioplasty of the left M1, M2, and A1 segments was performed (Figure 13-38 B,).
After the procedure, the patient recovered speech reception and arm function. On follow-up 3 months later, she only had mild hesitancy and paraphasic errors of speech. MRI displayed focal laminar necrosis and gliosis in the left MCA territory (Figure 13-38 C,
A 42-year-old woman with history of smoking underwent CT of the brain after an assault and was incidentally found to have a small anterior communicating aneurysm (Figure 13-39 A,). On MRI, the aneurysm projected into the right frontal lobe and was surrounded by a small area of gliosis (Figure 13-39 B,).
Four months later, the patient underwent CT angiography, which confirmed the presence of an aneurysm originating from the left anterior cerebral artery and measuring 11 by 5 mm (Figure 13-40 A–D,).
Her treatment was delayed for personal reasons, and 2 months later, she developed a severe headache, nausea, and vomiting associated with mild lethargy. Repeat CT scan of the brain showed a large right frontal hemorrhage and subarachnoid hemorrhage (Figure 13-41).
Catheter angiography (Figure 13-42 A,) and 3D DSA (Figure 13-42 B,) showed a number of small branches originating from the base of the left anterior cerebral artery aneurysm. The aneurysm was successfully coiled (Figure 13-42 C,), deliberately leaving a remnant at the base to protect these branches. The patient developed moderate ultrasonographic vasospasm and was treated with hemodynamic augmentation therapy. She was discharged home on postbleed Day 12 with good functional status.
ARTERIOVENOUS MALFORMATIONS
General Concepts
Natural History
105 – patient’s age in years.
TABLE 13-2 Spetzler-Martin arteriovenous malformation grading system.89
| Description | Points |
|---|---|
| Size (cm) | |
| < 3 | 1 |
| 3–6 | 2 |
| > 6 | 3 |
| Eloquence | |
| Yes | 1 |
| No | 0 |
| Deep venous drainage | |
| Yes | 1 |
| No | 0 |
Treatment Options
Current treatment approaches for AVMs include microsurgical resection alone, preoperative endovascular embolization followed by microsurgical resection, stereotactic radiosurgery alone, preprocedural endovascular embolization followed by radiosurgical treatment (Figure 13-44), and endovascular embolization only. However, it is important to remember that observation may be the best approach in some cases.
Decision making is complex and depends on size, location, and drainage. The Spetzler-Martin grade combines these factors to compose a frequently used score (Table 13-2).
Embolization
Radiosurgery
A 24-year-old woman previously evaluated for confusional episodes at age 15 presented to the emergency department with refractory headaches. She was found to harbor a right dorsal frontal AVM measuring 3.5 cm in maximal diameter; the lesion had deep venous drainage. CT scan of the brain and lumbar puncture did not disclose intraparenchymal or subarachnoid hemorrhage. Angiography showed no flow-related aneurysm. Two months later the patient developed rapidly progressive left hemiparesis. Repeat CT scan and CT angiography revealed a right external capsule hemorrhage located caudal to the nidus of the AVM (Figure 13-46). A flow-related aneurysm from a small insular feeder was seen on CT angiogram and subsequently confirmed by 3D angiography.
DURAL ARTERIOVENOUS FISTULAS
General Concepts
Cranial Dural Arteriovenous Fistulas
Cavernous Dural Arteriovenous Fistulas
TABLE 13-3 Barrow classification of carotid-cavernous sinus arteriovenous fistulas104
| Type A | Direct, usually traumatic or iatrogenic, high-flow shunts between the internal carotid artery and the cavernous sinus |
| Type B | Dural shunts between meningeal branches of the internal carotid artery and the cavernous sinus |
| Type C | Dural shunts between meningeal branches of the external carotid artery and the cavernous sinus |
| Type D | Dural shunts between meningeal branches of both the internal and external carotid arteries and the cavernous sinus |
Extracavernous Dural Arteriovenous Fistulas
Classification and Presentation
The most common clinical presentation of extracavernous dural arteriovenous fistulas is with intracranial hemorrhage. However, ischemic infarctions may also occur (Figure 13-51).
Hemorrhagic Risk
Treatment
A 60-year-old man was found poorly unresponsive at his house without evidence of trauma, intoxication, or coagulopathy. CT scan of the head revealed a large left frontal hemorrhage, a small right temporal hemorrhage, and a right subdural hematoma (Figure 13-55 A,).
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