Classifications of Cerebellar Hemangioblastomas Based on the Venous Drainage System
The present study proposed an anatomical classification of cerebellar hemangioblastomas based on the venous drainage system. Identification of the exact origin of the tumor is essential for optimum selection of the surgical approach for cerebellar hemangioblastomas, but determination on only preoperative MR images may be difficult due to deformation of the cerebellar surface by the tumor, peritumoral cyst, and perifocal edema, especially with larger tumors. Our classification found a strikingly limited subset of a unique drainage system relative to the tumor origin in all hemangioblastomas. This unique drainage system consisted of peculiar large inherent veins located at the origin of the cerebellar hemangioblastoma and forming the main drainage passing into specific dural venous sinuses. Such a drainage system passing through a single large draining vein into one of the venous sinuses is similar to the patterns found in arteriovenous malformations (AVMs).[35,36]
Cerebellar hemangioblastomas arise at various sites in the cerebellum with characteristic vascular architectures. The main histopathological feature of hemangioblastomas is the presence of two main components consisting of neoplastic stromal cells and abundant vascular cells. Recent studies demonstrated that these stromal cells represent the cytologic equivalent of embryonal hemangioblasts, which are common progenitor cells with differentiation potential into endothelial cells and hematopoietic stem cells.[6,31,32] Precirculatory vascular plexuses derived from hemangioblastic cell islands eventually establish communication through the arterial and venous systems. The nature of the active process remains unknown, but such an embryonal vascular plexus might connect to the regional draining veins emptying into the adjacent venous sinuses.
The classification of the cerebellar veins is based on three cortical surfaces, containing the superior hemispheric and superior vermian veins from the tentorial surface, inferior hemispheric and inferior vermian veins from the suboccipital surface, and petrosal veins from the petrosal surface. These superficial cerebellar veins terminate as bridging veins collecting into three major venous systems, the galenic, petrosal, and tentorial venous systems. The superficial veins of the galenic group include the precentral cerebellar veins, the superior vermian vein, and the anterior group of the superior hemispheric vein, that drain the anterior part of the tentorial surface. The petrosal draining group includes the superficial veins that drain the lateral part of the cerebellar hemisphere, collecting into the SPSs. The tentorial draining group includes the superficial veins draining the suboccipital surface and the posterior part of the tentorial surface, which collect into the straight and the transverse sinuses and the torcula, either directly or through a tentorial sinus. The cerebellar tonsil has two unique but different drainage systems. The superficial venous system includes the superior and inferior retrotonsillar veins which join to form the inferior vermian vein, emptying into the transverse sinuses and the torcula. The deep venous system including the supratonsillar veins drains into the vein of the cerebellomedullary fissure anastomosing with the vein of the inferior cerebellar peduncle, which directly drains into the jugular bulb or into the SPS via the vein of the middle cerebellar peduncle.[22,23] Accordingly, we proposed the anatomical classification of cerebellar hemangioblastomas based on the venous drainage system, and indicated the appropriate surgical approach. In our series, suboccipital and tentorial hemangioblastomas were associated with the tentorial draining group from the suboccipital surface and the posterior part of the tentorial surface, respectively. Petrosal and quadrigeminal hemangioblastomas were associated with the petrosal draining group and the galenic group, respectively. Tonsillar hemangioblastoma was separately categorized from the suboccipital type because of the association with a deep venous drainage system.
Surgery for hemangioblastomas is regarded as difficult due to their AVM-like characteristics.[15,21] Venous drainage and eloquence are key components of the Spetzler-Martin grading system, but these factors are not a reliable indicator of surgical risks of cerebellar AVM because of the specific anatomical properties of the cerebellum. Tumor location and supplementary grading system are important for predicting outcomes after cerebellar AVM resection. However, the most recent data from multicenter retrospective analysis indicated a significantly greater risk for poor outcomes in patients with deep venous drainage into the galenic system, which is an excellent indicator of cerebral AVM depth in the Spetzler-Martin grading system. Cerebellar AVMs can be classified into 5 subtypes, vermian, suboccipital, tentorial, petrosal, and tonsillar according to their location. This anatomical classification might be adapted to cerebellar hemangioblastomas, because the drainage system might consist of unique large venous drainage similar to cerebellar AVMs.[35,36]
Selection of the Surgical Approach
Safe resection of hemangioblastomas requires careful selection of the surgical approach to achieve panoramic exposure which allows early identification of the major feeding arteries and single main draining vein, and direct visualization of any small feeding arteries around the entire pial border, especially for large, solid tumor with deep location. Posterior fossa hemangioblastomas can be divided into four types according to their location and feeding arteries. Type I is found in the cerebellar hemisphere and vermis fed by the SCA, PICA, and AICA, type II in the cerebellar tonsil fed by the AICA, PICA, and meningeal branches, type III in the fourth ventricle and brain stem fed by the PICA, and type IV in the superior vermis fed by the SCA and meningeal branches. The suboccipital ipsilateral approach, modified far-lateral approach, suboccipital midline approach, and suboccipital supracerebellar approach are applied to tumor types I, II, III and IV, respectively.[5,33] In our experience, the anatomy of the arterial blood supply is not important to select the surgical approach because most large, solid hemangioblastomas receive multiple arterial blood supplies around the entire tumor-pial border or tumor-neural tissue interface from the SCA, AICA, and PICA, regardless of tumor origin and location in the cerebellum. Selection of surgical approach according to venous drainage system is important because this characteristic exclusively reflects the tumor origin.
Suboccipital hemangioblastomas were most common type (47.4%) in this study. Cerebellar hemangioblastomas predominantly located in posterior half of the cerebellum. Suboccipital hemangioblastoma is most accessible and can be excised through standard suboccipital craniotomy matching the tumor size and location. Tentorial hemangioblastomas were second most common type (21.1%) in this study, and could be resected through the OTA or SCITA to gain access to the entire tumor-pial margin on the superior cerebellar surface. Quadrigeminal hemangioblastomas were found in 10.5% of cases in this study. This type of hemangioblastoma is the most challenging because of the deepest location in the superior vermis and anteromedial region of the superior cerebellum facing the quadrigeminal plate, accessed through the OTA.
The preferred surgical approach to the upper, anterior part of the cerebellum is still controversial. The OTA and SCITA are the most commonly used among the various reported surgical approaches[5,7-9,11,20,24,26,27,33] and the subtemporal transtentorial approach is used for some limited cases.[2,3] We performed the OTA for 3 tentorial and 2 quadrigeminal hemangioblastomas with midline location, and the SCITA for one tentorial hemangioblastomas with lateral extension. We preferentially used the OTA for tentorial and quadrigeminal hemangioblastomas, because of the excellent, panoramic exposure of the entire tumor-pial border on the superior cerebellar surface, early management of the SCA, and direct visualization of the draining veins into the straight sinus or galenic system throughout surgery. Injury of venous drainage system is important to avoid during incision of the tentorium. In this study, the cerebellar hemispheric veins drained directly into the straight sinus, and no lesions had direct drainage into the tentorial sinus, but the OTA may not be feasible in such cases. Risk of retraction injury of the occipital lobe can be reduced by using gravity dependent and/or intermittent retraction. The SCITA was applied for tumors with tentorial sinus drainage or lateral extension of more than 35 mm and contralateral extension of more than 17 mm from the midline, which is the limit of the OTA. Petrosal hemangioblastoma was found in 10.5% of cases in this study, but may also include the rarely reported so-called cerebellopontine angle hemangioblastoma, so little information is available about the details of the venous drainage system. We treated petrosal hemangioblastomas through retrosigmoid craniotomies with exposure of the transverse-sigmoid junction to gain access to the petrosal surface and SPS, as previously reported.[1,15,21,24] Tonsillar hemangioblastomas were found in 10.5% of cases in this study. Midline suboccipital craniotomy including the posterior lip of the foramen magnum as well as the posterior arch of C1 could provide wide exposure of the dissection plane and allow access to the deep drainage system at the bottom of the tumor adjacent to the lateral recess of the fourth ventricle.
This study showed that improvement or stable symptoms and condition relative to preoperative findings were observed in 94.1% of patients and hydrocephalus was resolved in all cases. A previous study demonstrated that stable or improved conditions were found immediately after 88% of tumor resections and hydrocephalus resolved in 94% of patients after selective tumor resection. One patient in our series had poor outcome, who experienced intratumoral hemorrhage immediately after the preoperative liquid embolization with NBCA. This procedure is useful and important for reduction of arterial blood supply and intraoperative bleeding,[16,17,29,30] but formidable, severe embolic complications have been reported due to the unique properties of the posterior fossa. Surgery after preoperative liquid embolization on the same day is safe and effective for solid cerebellar hemangioblastoma. The timing of surgery and optimal indication should be considered to prevent any complication due to tumor swelling, intratumoral hemorrhage, or adjacent cerebellar infarction after preoperative embolization. No major complications occurred related to the surgical procedures and no single approach had a significantly higher incidence of postoperative neurological deficits. Therefore, no patient had experienced recurrence of the resected lesions at the last follow-up visit. Our classification based on the venous drainage system might be beneficial and helpful to select the optimal surgical approach for cerebellar hemangioblastomas, especially larger tumor with extensive perifocal edema.