1  Cerebrovascular Anatomy and Implications for Arteriovenous Malformation Treatment

W. Caleb Rutledge and Michael T. Lawton

Abstract

Arteriovenous malformations (AVMs) are complex vascular lesions. The Spetzler–Martin system and Lawton–Young supplementary grading scale are used to categorize AVMs and select patients for surgery. However, organizing AVMs into types and subtypes based on their location in the brain, arterial supply, draining veins, and eloquent structures allows for a unique surgical strategy for each AVM. There are seven AVM types based on their location in the brain: frontal AVMs, temporal AVMs, parieto-occipital AVMs, ventricular or periventricular AVMs, and AVMs in the deep central core, brainstem, and cerebellum. Each type comprises four to six subtypes based on their surgical anatomy, allowing for a tailored surgical approach and resection strategy.

Keywords: arteriovenous malformation, Spetzler–Martin, supplementary

1.1  Introduction

Brain arteriovenous malformations (AVMs) are complex vascular lesions with varying feeding arteries, draining veins, and niduses distributed throughout the brain. The Spetzler–Martin system and supplementary grading scales have long been used to categorize AVMs, as well as predict outcomes after AVM surgery and guide patient selection for surgery. However, AVM surgery requires a multitude of approaches, tailored to each AVM’s unique anatomy. Other than superficial AVMs immediately apparent on the brain’s surface, AVMs may require transsylvian, interhemispheric, skull base, or transtorcular approaches. Organization of AVMs into types and subtypes based on surgical anatomy allows for a unique surgical strategy for each AVM.¹

There are seven AVM types based on their location in the brain: frontal AVMs, temporal AVMs, parieto-occipital AVMs, ventricular or periventricular AVMs, and AVMs in the deep central core, brainstem, and cerebellum. Each type is further divided into four to six subtypes depending on the brain surface the AVM is based (i.e., lateral, medial, basal) or other specific anatomy (i.e., midbrain, pons, medulla). Each subtype has a unique arterial supply, draining veins, eloquent structures, surgical approaches, and resection strategy.

1.2  Frontal Arteriovenous Malformations

The frontal lobe has four surfaces: lateral, medial, basal, and sylvian. Frontal AVMs are supplied by branches from the superior trunk of the middle cerebral artery (MCA), including the orbitofrontal, prefrontal, precentral, and central arteries, as well as branches from the anterior cerebral artery (ACA), including the orbitofrontal, frontopolar, callosomarginal, anterior internal frontal, middle internal frontal, posterior internal frontal, paracentral, and pericallosal arteries. On the lateral and medial convexity, cortical veins ascend to the superior sagittal sinus (SSS). Veins from the sylvian and basal surfaces descend to the inferior sagittal sinus (ISS) and deep sylvian veins that continue to the basal vein of Rosenthal. Eloquent structures in the frontal lobe include the motor strip and Broca’s area in the dominant hemisphere.

1.2.1  Subtypes

There are five frontal AVM subtypes: the lateral frontal, medial frontal, paramedian frontal, basal frontal, and sylvian frontal. Lateral frontal AVMs are the most common subtype. These are stereotypical cone-shaped AVMs that extend toward the ventricle (► Fig. 1.1a). They are fed by MCA cortical branches ascending from the sylvian fissure to the inferior margin of the AVM. Venous drainage is superficial to the SSS. Lateral frontal AVMs may include eloquent structures such as the motor strip posteriorly and Broca’s area in the dominant hemisphere. Lateral frontal AVMs are easily exposed with a unilateral frontal craniotomy.

Medial frontal AVMs are visible only after opening the interhemispheric fissure and may be superficially based in the superior frontal gyrus or deep in the cingulate gyrus (► Fig. 1.1b). ACA branches feed medial frontal AVMs. Drainage is usually ascending to the SSS, but large medial frontal AVMs or those in the cingulate gyrus may have descending drainage to the ISS. Medial frontal AVMs may involve the motor strip posteriorly. Unlike lateral frontal AVMs, medial frontal AVMs are more difficult to expose and require a bifrontal craniotomy with opening of the interhemispheric fissure and gravity retraction to expose the medial surface of the frontal lobe.

Paramedian frontal AVMs are a combination of lateral and medial frontal subtypes and occupy two surfaces of the frontal lobe (► Fig. 1.1c). Unlike other frontal subtypes, cortical branches from two arterial territories, the MCA and ACA, supply paramedian AVMs. Venous drainage is to the SSS. Similar to lateral and medial frontal AVMs, paramedian AVMs involve the motor strip when they are posteriorly located. Paramedian AVMs also require a bifrontal craniotomy to expose, but gravity retraction is avoided to preserve access to the lateral convexity.

Basal frontal AVMs are located along the anterior cranial fossa floor in the lateral orbital gyri or medially in the gyrus rectus and olfactory apparatus (► Fig. 1.1d). Basal frontal AVMs are fed by MCA branches posterolaterally and ACA branches anteromedially. Venous drainage is usually superficial to the SSS, but may be deep to the basal vein of Rosenthal. Basal frontal AVMs are considered noneloquent, but care should be taken to preserve the olfactory apparatus and its blood supply. Basal frontal AVMs are exposed with an orbital-pterional craniotomy.

Sylvian frontal AVMs are located in the pars orbitalis, pars triangularis, and pars opercularis of the inferior frontal gyrus and the frontal operculum (► Fig. 1.1e). They are supplied by M3 branches rather than cortical MCA branches, and drained by superficial and deep sylvian veins. As they are based in the pars opercularis and pars triangularis comprising Broca’s area, sylvian frontal AVMs are highly eloquent. They are exposed with a standard pterional craniotomy.

1.3  Temporal Arteriovenous Malformations

The temporal lobe also has four surfaces: lateral, basal, sylvian, and medial. Blood supply is from proximal M1 branches, the temporopolar and anterior temporal arteries coursing inferiorly to the temporal pole, and branches from the inferior trunk of the MCA, including middle temporal, posterior temporal, temporo-occipital, and angular arteries, descending from the sylvian fissure to the lateral surface of the temporal lobe. Branches from the P2 segment of the posterior cerebral artery (PCA), the hippocampal and posterior temporal arteries, supply the basal surface of the temporal lobe. Finally, the anterior choroidal artery supplies the choroid plexus of the temporal horn of the lateral ventricle. Venous drainage of the temporal lobe is complex, with drainage to the sphenoparietal sinus anteriorly, posteriorly to the vein of Labbé and transverse sinus, medially to the basal vein of Rosenthal and galenic system, and superiorly to sylvian veins and SSS. Eloquent structures in the temporal lobe include Wernicke’s area in the dominant hemisphere, Heschl’s gyrus, the hippocampus and parahippocampus, and optic radiations.

1.3.1  Subtypes

There are four temporal AVM subtypes: lateral temporal, basal temporal, sylvian temporal, and medial temporal. The lateral temporal subtype is the most common (► Fig. 1.2a). Its blood supply is from the inferior trunk of the MCA descending from the sylvian fissure to the superior border of the AVM. Feeders from the temporopolar and anterior temporal arteries may course around the temporal pole to its anterior border, while branches from the PCA occasionally feed posteriorly located lateral temporal AVMs. Drainage is usually superficial to the vein of Labbé and transverse sinus. Lateral temporal AVMs may involve Wernicke’s area when they are posteriorly located in the dominant hemisphere. Like lateral frontal AVMs, lateral temporal AVMs are easy to expose using a pterional craniotomy for AVMs in front of the external auditory canal and a temporal craniotomy for those behind the external auditory canal.

Basal temporal AVMs are based in the inferior temporal gyrus, fusiform gyrus, and parahippocampal gyrus (► Fig. 1.2b). P2 PCA branches emanating from the crural and ambient cistern supply the AVM’s medial border. MCA feeders may descend and wrap around the inferior temporal gyrus to its lateral border. Basal temporal AVMs also often have meningeal feeders from the dura of the middle fossa floor. Drainage is usually superficial, but may be deep to the basal vein of Rosenthal. There are no eloquent structures on the basal temporal surface. A temporal craniotomy is used to expose basal temporal AVMs. They are not visible on the lateral surface and require a subtemporal approach and dissection.

Sylvian AVMs are supplied by MCA M3 opercular branches (► Fig. 1.2c). Additionally, the anterior choroidal artery may supply the medial margin. Venous drainage is usually superficial to sylvian veins. Sylvian AVMs may involve Heschl’s gyrus or Wernicke’s area when they are posteriorly located in the dominant hemisphere. Similar to sylvian frontal AVMs, temporal sylvian AVMs are exposed though a standard pterional craniotomy and transsylvian dissection.

Medial temporal AVMs involve the uncus, parahippocampal gyrus, and hippocampus (► Fig. 1.2d). Feeders from the anterior choroidal artery and branches of the P2 PCA supply the medial and posterior borders. Anteriorly located medial temporal AVMs may have supply from the temporopolar and anterior temporal artery, while posteriorly located ones tend to have PCA supply. Additionally, thalamoperforators from the posterior communicating artery may contribute. Venous drainage is deep to the basal vein of Rosenthal. Medial temporal AVMs are eloquent given they involve the hippocampus and memory function. Exposure of these AVMs is challenging. An orbitozygomatic craniotomy and a deep transsylvian dissection along the anterior choroidal artery are required to mobilize the temporal lobe away from the frontal lobe and afford a limited view at best. More posteriorly located medial temporal AVMs require a transcortical transventricular approach if the transsylvian view is inadequate.

There are four parieto-occipital subtypes: lateral parieto-occipital, medial parieto-occipital, paramedian, and basal occipital. The lateral parieto-occipital AVM is one of the most common AVMs and often has a cortical base with a tapered extension toward the ventricle (► Fig. 1.3a). MCA cortical arteries mainly supply them. Drainage is superficial, ascending to the SSS or descending to sylvian veins. Parieto-occipital AVMs are eloquent when located in the postcentral gyrus, visual cortex, or angular or supramarginal gyrus. They are exposed with a simple convexity craniotomy. There is no need to cross a sinus or expose the interhemispheric fissure or undersurface of the occipital lobe.

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