Surgical Treatment of Cerebellar Arteriovenous Malformations

15 Surgical Treatment of Cerebellar Arteriovenous Malformations

João Paulo Almeida, Vitor Yamaki, Mateus Reghin Neto, Feres Chaddad Neto, Albert Rhoton Jr., and Evandro de Oliveira

Abstract

Cerebellar arteriovenous malformations (AVMs) represent approximately 10% of all intracranial AVMs. Although less common, these lesions are associated with rates of hemorrhage, morbidity, and mortality higher than supratentorial AVMs. In this chapter, we evaluate the anatomical characteristics of the cerebellum and cerebellar AVMs and discuss the application of a new classification of cerebellar AVMs based on the microsurgical anatomy of this region. The smaller size of the cerebellum, the lack of perforating arteries and deep venous drainage system, and few eloquent areas when compared to the brain hemispheres are important characteristics to be considered for planning and treatment of cerebellar AVMs. Therefore, we propose an anatomical classification system for cerebellar AVMs based on size (< 2 cm: I; 2–4 cm: II; > 4 cm: III), location (superficial: A; deep: B; mixed: C), and extension to the dentate nucleus and superior cerebellar peduncles. The anatomical classification of cerebellar AVMs may be used for planning of microsurgical treatment of different types of AVMs in this region.

Keywords: arteriovenous, malformation, cerebellum, surgery, classification, anatomy

Key Points

Cerebellar arteriovenous malformations (AVMs) present specific natural history, clinical presentation, and anatomical characteristics.
Hemorrhage of these lesions is associated with high rates of morbidity and mortality, which justifies the importance of their adequate treatment.
Microsurgical resection is the gold standard treatment of cerebellar AVMs.
Size, location, and involvement of the dentate nuclei play a major role in the surgical planning of cerebellar AVMs.

15.1 Introduction

Posterior fossa arteriovenous malformations (AVMs) account for 7 to 15% of all intracranial AVMs¹^,²^,³^,⁴ and are mostly represented by cerebellar AVMs, a heterogeneous group that includes 75 to 81.2% of all the posterior fossa AVMs.³^,⁴ Even though cerebellar AVMs represent a minority of all intracranial AVMs, they carry a higher risk of rupture and are associated with considerable higher rates of morbidity and mortality.²

Cerebellar AVMs, unlike supratentorial malformations, present more frequently with hemorrhages.² Mortality rates of up to 66.7% have been associated with the rupture of posterior fossa AVMs.⁵ Hernesniemi et al performed a retrospective analysis of 238 AVM patients with a mean follow-up period of 13.5 years.⁶ According to this study, an infratentorial location is one of the most important risk factors for rupture. Univariate analysis demonstrates an annual rate of rupture of 11.6% in the first 5 years after admission, with a cumulative rupture rate of 45% in the first 5 years, as compared with an annual rate of 4.3% and a cumulative 5-year rate of 19% for supratentorial AVMs.

Microsurgical resection remains the gold standard treatment for cerebellar AVMs. Treatment selection must be performed according to the characteristics of each case, and the complete resection of the AVM must be the goal of treatment. Surgery is associated with excellent outcomes when performed by a dedicated vascular microneurosurgeon,⁴^,⁷^,⁸^,⁹ with reported rates of complete resection of 92 to 100% and morbidity and mortality of 9 to 17% and 4 to 8%, respectively.⁴^,⁵^,⁷^,⁸^,⁹^,¹⁰^,¹¹

In this chapter, we aim to discuss the microsurgical anatomy of cerebellar AVMs and surgical techniques for resection of those lesions.

15.2 Methodology

The cerebellar anatomy review was based on analysis of studies from the Microsurgery Laboratory of the University of Florida, Gainesville, and the Microsurgery Laboratory of the Institute of Neurological Sciences–Hospital Beneficencia Portuguesa de Sao Paulo.

Based on the microsurgical anatomy of the cerebellum and posterior fossa, our philosophy for treatment of cerebellar AVMs is discussed through evaluation of selected cases treated by our team.

15.3 Results

15.3.1 Microsurgical Anatomy

The exquisite complexity of posterior fossa contents requires a thorough knowledge of microsurgical anatomy of this region. Such anatomic background guides the surgeon to the most appropriate approach.⁷^,¹² Only then the surgeon is able to adequately evaluate the spatial location of the malformation (i.e., its relationships within the cerebellum and/or brainstem to the posterior fossa cranial nerves, arteries, and veins) based on the preoperative catheter digital subtraction angiography (DSA), magnetic resonance imaging (MRI) scans, and computed tomography (CT) scans.¹³

Anatomically, the cerebellum may be divided into three surfaces: tentorial, petrosal, and suboccipital.¹⁴ Each of these is related with a cerebellar fissure, cerebellar artery, and specific draining veins. As described by Yasargil,¹⁵ knowledge of this anatomy is crucial since arterial supply and venous drainage of AVMs usually follow the same vascular pattern of normal brain, which guides the surgeon during resection of the lesion.

The tentorial surface faces and conforms to the lower surface of the tentorium¹⁴ (► Fig. 15.1). The anteromedial part of this surface, the apex, formed by the anterior vermis, is the highest point on the cerebellum. This surface slopes downward from its anteromedial to its posterolateral edge. On the tentorial surface, the transition from the vermis to the hemispheres is smooth and not marked by the deep fissures on the suboccipital surface between the vermis and hemispheres. The cerebellomesencephalic or precentral cerebellar fissure is located between the posterior aspect of the midbrain and the tentorial surface, closely related with the upper roof of the IV ventricle. The superior cerebellar artery is mainly responsible for the arterial supply of this region ¹⁶ (► Fig. 15.2). The superior cerebellar artery (SCA) is the last branch of the basilar artery before its bifurcation into the posterior cerebral arteries. It arises in front of the midbrain, near the pontomesencephalic junction, below the oculomotor nerves; it runs toward the posterior surface of the brainstem, passing inferior to the trochlear (IV) nerve and superior to the trigeminal (V) nerve, encircling the midbrain. It then reaches the cerebellomesencephalic fissure, giving rise to the precerebellar arteries. After reaching this region, the SCA sends cortical branches to the tentorial surface of the cerebellar hemispheres and to the vermis. The venous drainage of the tentorial region is performed by the superior hemispheric and vermian veins, which drain toward the vein of Galen, torcula, and transverse sinuses (► Fig. 15.3).

Fig. 15.1 Tentorial surface of the cerebellum. 1: primary fissure; 2: culmen; 3: cerebellomesencephalic fissure; 4: postclival fissure; 5: superior semilunar lobule; 6: declive. (Images from the personal collection of Dr. Evandro de Oliveira. Obtained at the Laboratory of Microneurosurgery, Dr. Albert Rhoton Jr, University of Florida, Gainesville.)

Fig. 15.2 Cerebellomesencephalic and cortical segments of the ACS. 1: hemispheric branches; 2: vermian branches; 3: precerebellar branches. (Images from the personal collection of Dr. Evandro de Oliveira. Obtained at the Laboratory of Microneurosurgery, Dr. Albert Rhoton Jr, University of Florida, Gainesville.)

Fig. 15.3 (a,b) Venous drainage of the cerebellum. Superior hemispheric and vermian veins drain the tentorial surface of the cerebellum, while anterior hemispheric veins are the main responsible for the drainage of the petrosal surface and inferior vermian and hemispheric veins for the suboccipital surface. (Images from the personal collection of Dr. Evandro de Oliveira. Obtained at the Laboratory of Microneurosurgery, Dr. Albert Rhoton Jr, University of Florida, Gainesville.)

The petrosal or anterior surface faces the posterior surface of the petrous bones, the brainstem, and the fourth ventricle¹⁴ (► Fig. 15.4). The lateral or hemispheric part of the petrosal surface rests against the petrous bone and is retracted to expose the cerebellopontine angle (CPA). The median or vermian part of the petrosal surface has a deep longitudinal furrow, the anterior cerebellar incisura, which wraps around the posterior surface of the brainstem and fourth ventricle. The right and left halves of the petrosal surfaces are not connected from side to side by a continuous strip of vermis, as are the suboccipital and tentorial surfaces, because of the interposition of the fourth ventricle between the superior and inferior part of the vermis. The cerebellopontine fissure is formed by the folding of the cerebellar hemisphere around the lateral side of the pons and the middle cerebellar peduncle. It has a superior limb between the rostral half of the middle cerebellar peduncle and the superior part of the petrosal surface and an inferior limb between the caudal half of the middle cerebellar peduncle and the inferior part of the petrosal surface. The middle cerebellar peduncle fills the interval between the two limbs. The anterior inferior cerebellar artery (AICA) is the main arterial trunk related to the cerebellopontine fissure and petrosal surface of the cerebellum ¹⁶ (► Fig. 15.5). It originates anterior to the pons and runs in a posterolateral direction, in close association to the facial (VII) and vestibulocochlear (VIII) nerves in the CPA. After passing around the flocculus, it reaches the cerebellopontine fissure and then sends cortical branches to the petrosal surface of the cerebellum. The anterior hemispheric veins and the superior petrosal sinus are primarily responsible for the venous drainage of this region.

Fig. 15.4 Petrosal surface of the cerebellum. 1: facial and vestibulocochlear nerves; 2: flocculus; 3: superior semilunar lobule; 4: petrosal fissure; 5: quadrangular lobule; 6: inferior semilunar lobule; 7: biventral lobule. (Images from the personal collection of Dr. Evandro de Oliveira. Obtained at the Laboratory of Microneurosurgery, Dr. Albert Rhoton Jr, University of Florida, Gainesville.)

Fig. 15.5 Irrigation of the petrosal surface of the cerebellum. 1: anterior pontine segment of the AICA; 2: lateral pontine segment of the AICA; 3: flocculus; 4: floculopeduncular segment of the AICA; 5: cortical segment of the AICA; (Images from the personal collection of Dr. Evandro de Oliveira. Obtained at the Laboratory of Microneurosurgery, Dr. Albert Rhoton Jr, University of Florida, Gainesville.)

The suboccipital surface of the cerebellum, located between the sigmoid sinuses and below the transverse sinus, is the most complex of the three surfaces¹⁴ (► Fig. 15.6). The suboccipital surface presents a deep vertical cleft, the posterior cerebellar incisura. The vermis is folded into it and forms the cortical surface within this incisura. The lateral walls of the incisura are formed by the medial aspects of the cerebellar hemispheres. At the suboccipital surface, the vermis is located posterior to the fourth ventricle and above the foramen of Magendie. In this region, the superior portion of the vermis presents a pyramidal shape and it is, therefore, named pyramid. The inferior portion, the uvula, projects downward between the cerebellar tonsils, presenting a similar configuration to that observed at the oropharynx. The rostromedial borders of the tonsils are in close contact to the lateral borders of the uvula. The nodule, located deep to the uvula, is related to the inferior half of the fourth ventricle roof. The broadest portion of the vermis in the posterior cerebellar incisura is the pyramid–uvula junction. Inferiorly, the incisura is continuous with the vallecula cerebelli, a cleft between the tonsils that communicates with the foramen of Magendie. Located between the suboccipital surface of the cerebellum and the medulla, the cerebellomedullary fissure is one of the most complex fissures of the human brain. Its ventral wall is formed by the inferior medullary velum, posterior surface of the medulla, and tela choroidea. The posterior wall is composed by the uvula, tonsils, and biventral lobules. It extends superiorly to the level of the lateral recesses and communicates around the superior poles of the tonsils with the cisterna magna, through the foramen of Magendie with the fourth ventricle, and around the foramina of Luschka with the cerebellopontine fissures. The posterior inferior cerebellar artery (PICA) is the main vessel for arterial supply of the suboccipital region¹⁶ (► Fig. 15.7). It originates from the distal portion of the intracranial vertebral artery, anterior to the medulla. It encircles the inferior portion of the brainstem, passing close to the hypoglossal (XII) nerve and, then, to the glossopharyngeal (IX), vagus (X) and spinal accessory (XI) nerve. It then usually forms a caudal and a cranial loop medially to the tonsil and finally reaches the cerebellomedullary fissure, close to the lower portion of the roof of the fourth ventricle. Once out of this fissure, PICA sends cortical branches to the inferior vermis, tonsils, and the suboccipital surface of the cerebellum.¹²^,¹⁵ The venous drainage of this region is based on the inferior hemispheric and vermian veins, which drain toward the transverse and/or tentorial sinuses and torcula.

Fig. 15.6 Suboccipital surface of the cerebellum and its veins, after removal of the tonsils and biventral lobules. The inferior hemispheric and vermian veins are the main responsible for the drainage of this surface. (Images from the personal collection of Dr. Evandro de Oliveira. Obtained at the Laboratory of Microneurosurgery, Dr. Albert Rhoton Jr, University of Florida, Gainesville.)

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