AVMs of the Sylvian Fissure


Pearls

  • Sylvian fissure AVMs are very frequently related to eloquent cortex anatomically or by virtue of vascular anatomy.

  • Permanent morbidity after resection ranges from 0% to 34%.

  • Classification is based upon anatomical location within (pure sylvian) or around (perisylvian) the sylvian fissure and associated eloquent brain.

  • A multimodal approach (embolization, surgery, radiosurgery, observation) should be meticulously evaluated in cases of these high-risk lesions.

  • This AVM location requires discussion with the patient with regard to a multistaged approach.

Introduction

Supratentorial arteriovenous malformations (AVMs) are relatively rare pathological lesions, with an incidence of 1 in 100,000 persons per year. These lesions are responsible for 1%–2% of all strokes. AVMs within the sylvian fissure are rarer still; only 5%–10% of all intracranial AVMs (iAVMs) are identified within this location. While approximately half of the patients with sylvian AVMs present with hemorrhage, many present with seizures (20%–25%) due to the close proximity of these lesions to key epileptogenic brain regions in the mesial temporal lobe. Despite their location, the natural history and rupture risk of sylvian AVMs remain on par with those of AVMs in other supratentorial locations, but decision-making regarding treatment must account for adjacent structures, which alters the typical risk-benefit analysis. Given the proximity to key eloquent brain regions, including the basal ganglia, the internal capsule, the insula, Broca’s area, Wernicke’s area, and the arcuate fasciculus, treatment of this iAVM subtype presents unique challenges. Furthermore, sylvian AVMs are typically intertwined with middle cerebral artery (MCA) vessels, presenting additional challenges to identify pathologic vessels, preserve native MCA vessels, and minimize ischemic complications.

Sylvian AVM Classification

Initially described by Sugita et al. in 1987, sylvian fissure AVMs can fall into four categories, depending on their precise location within or around the sylvian fissure. This categorization includes pure (located within the confines of the sylvian fissure), lateral (adjacent temporal lobe and Wernicke’s area), medial (adjacent frontal lobe and Broca’s area), and deep (basal ganglia, internal capsule, and insula) sylvian fissure AVMs ( Table 34.1 ). While sylvian AVMs rarely fall into these categories in an isolated manner, classification provides a framework for discussion of the pitfalls and potential complications of various treatment modalities for these respective perisylvian locations.

Table 34.1
Sylvian Fissure AVM Categorization
Category Eloquent Parenchyma Involved
Pure NA
Lateral Wernicke’s area
Heschl’s gyrus
Medial Broca’s area
Inferior motor cortex
Deep Insula
Basal ganglia
Internal capsule
NA , Not applicable.

Given the proximity of sylvian AVMs to sensitive and critical brain structures, treatment poses significant risks regardless of the treatment modality employed. In addition to the aforementioned neighboring eloquent brain regions, the location within the sylvian fissure provides additional complexity due to the presence of numerous “en passage” MCA vessels, which must be meticulously identified and preserved whether the lesions are treated surgically or endovascularly. These en passage vessels drop branches to the AVM, while passing adjacent to the nidus and continuing onward to supply critical surrounding cortex. Although all sylvian AVMs are involved with the MCA vasculature to a degree, pure sylvian AVMs (located solely within the fissure) are intricately intertwined with the MCA candelabra. The nidus of pure sylvian AVMs is distinctly within the confines of the sylvian fissure, providing a plane of separation from the parenchyma by a natural pial barrier. This natural barrier allows resection of these lesions without invasion of normal parenchyma.

It is important to distinguish between pure sylvian AVMs and perisylvian AVMs, as operative and endovascular risks are dependent on the precise nidal location. Perisylvian AVMs are located in the parenchyma, immediately adjacent to the sylvian fissure, either in deep structures (insula, basal ganglia, internal capsule) or more superficial eloquent locations (Broca’s area, Wernicke’s area). Although most of the nidus is typically located within the brain parenchyma, portions of nidus are located within the fissure, and arterial input arises directly from the MCA. As perisylvian parenchymal lesions grow and evolve, they will often recruit additional arterial input from the MCA within the fissure, transitioning into combined lesions of the fissure and adjacent parenchyma. Treatment of perisylvian AVMs not only carries risk to the native MCA but also carries risk to the adjacent eloquent brain parenchyma. Pure sylvian AVMs, on the other hand, carry less risk to eloquent tissue but entail more difficulty in distinguishing between en passage vessels and nidal arterial input.

Despite these risks inherent in treating sylvian AVMs, the sylvian fissure does provide a natural corridor for approaching superficial and deep AVMs. While resection of insular, basal ganglia, and internal capsule lesions carries substantial risk, utilizing the sylvian fissure for the approach can mitigate approach-related morbidity to a degree. This may underlie previous reports, which have identified surgical success (operative resection without worsened neurologic function) to be as high as 85%–90%.

Treatment of Sylvian AVMs

Role of surgery

Resection of sylvian AVMs has been described for nearly four decades, with numerous case series demonstrating a high degree of efficacy and reasonable morbidity ( Table 34.2 ). Initially, resection of these lesions was reserved for patients with prior hemorrhage and significant neurologic deficits, but more recently, advances in microsurgery have allowed for a more aggressive approach in select patients. As previously discussed, the precise location of the AVM (pure sylvian or perisylvian) will significantly impact perioperative morbidity. Conventional angiography and MRI prior to potential resection are crucial for treatment decision and surgical planning. MRI can assist in the identification of the precise location of the lesion and potentially involved eloquent parenchyma. Further, while sylvian AVMs receive the large majority of their vascular supply from the MCA, additional arterial input from the anterior choroidal, posterior choroidal, and lenticulostriate arteries may be observed, rendering careful angiographic assessment essential prior to any potential treatment.

Table 34.2
Surgical Series Involving Pure Sylvian and Perisylvian AVM Resection
Authors and Year No. of Patients Morbidity Mortality
Heros, 1982 3 Transient 33%
Permanent 33%
0%
Sugita et al., 1987 16 Transient 81%
Permanent 6%
6%
Oka et al., 1990 3 Transient 33%
Permanent 33%
33%
Malik et al., 1996 24 Transient 33%
Permanent 17%
4.2%
Yamada et al., 1998 22 Transient 4.5%
Permanent 4.5%
0%
Zimmerman et al., 2000 8 Transient 50%
Permanent 0%
0%
Du et al., 2004 10 Transient 30%
Permanent 0%
0%
Lawton et al., 2007 28 Transient 14%
Permanent 3.6%
0%
Bostrom et al., 2011 20 Transient 15%
Permanent 10%
0%
Gabarros Canals et al., 2013 5 Transient 0%
Permanent 20%
20%
Lopez-Ojeda et al., 2013 5 Transient 0%
Permanent 20%
0%
Liu et al., 2013 41 Transient 44%
Permanent 34%
2.4%
Potts et al., 2013 48 Transient 6%
Permanent 6%
0%
Pabaney et al., 2014 7 Transient 20%
Permanent 20%
0%
Ding et al., 2018 1 None 0%

Once the decision to move forward with surgery is made, the precise location of resection will vary based on the nidal location, but all sylvian AVMs are approached with a wide sylvian fissure opening, typically utilizing a pterional craniotomy. Full fissure opening into the distal aspect of the sylvian fissure is necessary to completely skeletonize the MCA. This allows identification of the AVM arterial input, venous drainage, and nidus, but it also aids in clearly delineating the MCA and its branches as it courses through the fissure. Full anatomic exploration and identification of the native MCA and AVM vasculature are paramount prior to ligation of arterial input to the nidus in order to preserve all vessels providing blood supply to normal parenchyma.

Preservation of the parent MCA, en passage arteries, and perforating arteries limits neurologic morbidity from the procedure, although it is often difficult to parse out these different vessel types without full exposure. If there is any doubt about whether a vessel is feeding into the AVM or passing by, it should not be sacrificed until the nidus is fully exposed and a definitive assessment can be made. When AVM feeding arteries are relatively short or when the nidus is directly fed off the parent MCA, the use of suture or AVM clips is recommended to avoid coagulation damage to the native MCA. Particularly with medial sylvian AVMs, frequent use of clips, rather than cautery, is recommended, as partially cauterized vessels may retract into eloquent tissue, leading to a need for surgical manipulation of potentially eloquent areas that otherwise would be undisturbed.

The draining vein often lies within the sylvian fissure on top of the nidus, and care must be taken to preserve this structure until the nidus is ready to be removed. Venous drainage patterns tend to vary with sylvian AVM location. Pure sylvian AVMs typically drain superficially through the middle cerebral veins, whereas medial perisylvian AVMs and lateral perisylvian AVMs tend to drain through the veins of Trolard and Labbé, respectively. Deep sylvian AVMs typically exhibit deep venous drainage into the thalamostriate and internal cerebral veins. As with all AVMs, preservation of the draining vein until all arterial input has been ligated is of utmost importance.

In addition to preserving the native vasculature, minimizing manipulation of adjacent parenchyma is crucial in resection of perisylvian AVMs. Pure sylvian AVMs have no associated eloquent cortex, but medial sylvian AVMs border Broca’s area and the inferior aspect of the motor strip, lateral sylvian AVMs border Wernicke’s area and Heschl’s gyrus, and deep sylvian AVMs border the basal ganglia, internal capsule, and arcuate fasciculus. While perisylvian AVMs in the adjacent parenchyma may receive additional arterial supply from other vascular territories, such as anterior or posterior choroidal and lenticulostriate arteries, the vast majority of the arterial input arises from the MCA. In approaching perisylvian AVMs, it is recommended to prune all MCA arterial supply within the sylvian fissure prior to working around the parenchymal planes of the nidus. This allows resection to be maintained much tighter to the AVM nidus, thus reducing surgical morbidity from manipulation of eloquent cortex.

Numerous studies ( Table 34.2 ) have evaluated outcomes following resection of sylvian AVMs. Lawton et al. evaluated their series of sylvian AVMs, assessing 28 patients who underwent resection, 54% of whom presented with hemorrhage. Among this population, they observed transient neurologic deficits in 14% of the patients, but the rate of permanent neurologic morbidity was only 3.6%. No surgical mortality was observed, and 89% of the patients achieved good functional outcomes at a mean follow-up of 20 months. Similarly, Zimmerman et al. reported transient neurologic deficits in 50% of their patients, with all recovering within 3 months of surgery and no surgical mortality.

While resection of sylvian AVMs can at times be a safe and feasible option, it should be approached cautiously, appropriately weighing the risks and benefits of treatment. Factors such as age, history of rupture, eloquent cortex, insular locations, and involvement of lenticulostriate or anterior choroidal arteries need to be carefully considered prior to surgical intervention. Given these factors, a less aggressive approach with stereotactic radiosurgery (SRS) or even conservative observation may be in the patient’s best interest.

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