Acta Neurochir (Wien) (2007) 149: 399–406 DOI 10.1007/s00701-006-1091-z Printed in The Netherlands

Neurosurgical Technique Novel application of computer-assisted cisternal endoscopy for the biopsy of pineal region tumors: cadaveric study A. S. Youssef1 , J. T. Keller2, and H. R. van Loveren1 1 2

Department of Neurosurgery, University of South Florida, Tampa, Florida, USA Department of Neurosurgery, The Neuroscience Institute, University of Cincinnati College of Medicine and the Mayfield Clinic, Cincinnati, Ohio, USA

Received June 28, 2006; accepted December 8, 2006; published online February 26, 2007 # Springer-Verlag 2007

Summary Background. Long-standing debate continues about the management and biopsy of pineal tumors because of their complex microsurgical anatomy and deep location. Inspired by the concept of biopsy under direct visualization in the absence of hydrocephalus, we explored the effectiveness of neuroendoscope outside of its traditional territory using a new minimally invasive technique, computer-assisted cisternal endoscopy (CACE), for the biopsy of pineal tumors. Method. Five cadaver heads were dissected to expose the pineal region through the posterior fossa. In the other 5 heads, a rigid endoscope-wand combination was introduced in the supracerebellar space lateral to the arachnoid of the superior cerebellar cistern in midline. Endoscopic exposure of the pineal gland was correlated with the real-time image of the localizing wand. After the wand was removed, arachnoid was further dissected from the deep veins and the pineal gland, and a fourquadrant biopsy was obtained. Findings. The combination of technologies of frameless guided stereotaxy and neuroendoscopy enhanced our ability to navigate the ventriculoscope in narrow spaces (e.g., posterior fossa cisterns). Compared with transventricular and conventional stereotactic trajectories, application of CACE in supracerebellar infratentorial trajectory offered the shortest route to the pineal region, anatomical orientation, no violation of eloquent neurovascular structures, and adequate visibility to deep veins and arteries.

Conclusions. CACE may be used to approach pineal lesions outside the cerebral ventricular system for biopsy or debulking. Continuous computer updates on the endoscope position allows its safe navigation in narrow spaces (e.g., cerebrospinal fluid cistern). Its success will await future surgical trials. Keywords: Biopsy; cisternal endoscopy; endoscopy; pineal gland; pineal tumors. Introduction Tumors of the pineal gland are rare, accounting for 0.4–1% of intracranial tumors in European and American literature and 4% in the Japanese literature [1, 18]. Pineal tumors typically affect males (4:1) under 20 years of age [12]. More than 17 different tumor types arise from the pineal region, reflecting the complex and heterogeneous nature of this glandular tissue [6, 9, 11] (Table 1). Germinoma, which is the most common type, accounts for 43–70% and 21–44% of pineal region tumors in Japanese and American=European populations, respectively. Germinoma is followed by astrocytoma, teratoma, pineoblastoma, and others [12, 15, 16]. Pineal tumors lie deep within the cranium closely related to the deep venous system, which represents the cornerstone in selection of surgical approach to the pineal region. The complex microsurgical anatomy and deep location of this region continues to foster a longstanding debate about management of pineal tumors,

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Table 1. Pathological classification of pineal tumors (with permission from the University of South Florida) Tumor category

Specific types

Germ-cell tumors

germinoma (atypical teratoma), teratoma and teratoid tumors (dermoid and epidermoid), chorioepithelioma, embryonal carcinoma (EST or yolk sac carcinoma), rhabdomyosarcoma, combination of the above

Pineal parenchymal cell tumors

pinealblastoma (or pineoblastoma), pinealcytoma (or pineocytoma), pinealcytoma=blastoma

Tumors of supporting (glial stroma) or adjacent tissues

gliomas (astrocytoma, spongioblastoma, ependymomas, choroid plexus papilloma), ganglioneuroma and ganglioglioma, meningioma, hemangiopericytoma, chemodectoma, melanoma (malignant)

Non-neoplastic cysts and vascular lesions

degenerative cysts, arachnoid cysts, vascular lesions (aneurysm of vein of Galen, arteriovenous malformation, cysticercosis)

specifically the use of direct surgical treatment versus conservative irradiation with drainage procedures. The two worldwide surveys about pineal tumor management conducted in 1992 [12] and 1998 [13] identified the growing trend of obtaining histological diagnosis before radiotherapy and=or chemotherapy for several reasons. First, 36–50% of pineal tumors are either benign or radio-resistant. Second, radiation therapy exerts harmful effects on children with pineal tumors. Third, minimally invasive procedures (i.e., neuroendoscopy, stereotactic surgery, radiosurgery=radiation therapy) are widely accepted as safe neurosurgical treatments. Finally, identification of the exact histological type allows a more specific use of therapeutic tools, specifically radiation and new chemotherapeutic agents. Histological diagnosis for pineal region tumors is achieved through direct surgery or biopsy techniques. Direct surgery not only is curative for benign lesions but provides a generous amount for tissue biopsy. Closed biopsy techniques include stereotactic and neuroendoscopic biopsy. Stereotactic biopsy can be limited by inadequate amounts of specimen, especially for mixed tissue and rare cell types, which are difficult to interpret, increase the diagnostic error, and the risk of hemorrhage. Neuroendoscopic biopsy is more favorable in lesions associated with hydrocephalus; it often requires use of a flexible endoscope, which is sometimes technically difficult. In this cadaveric study, we evaluate the effectiveness of computer-assisted cisternal endoscopy (CACE) to overcome the above-mentioned limitations in the biopsy of pineal region tumors. A computer-assisted endoscopic technique previously applied for transventricular biopsy offered advantages including planning the entry point, localizing the ideal target trajectory, and obtaining an intraoperative computer update on the endoscope location [14]. In our microsurgical laboratory, we studied the anatomy of the pineal region in cadavers, incorporating stereotactic and neuroendoscopic advances into one biopsy technique that adds real-time neuroimag-

ing orientation to the navigating endoscope. Finally, we evaluated different surgical trajectories to the pineal region on the basis of the distance to the target, natural anatomical passages, and obstacles created by important neurovascular structures and eloquent brain tissue. We studied the use of the supracerebellar cistern as a new trajectory to navigate the neuroendoscope and biopsy the pineal gland with this minimally invasive technique. Methods and materials Cadaveric preparation In 10 cadaver heads, both the internal carotid arteries, vertebrobasilar system, and jugular veins were cannulated and irrigated with warm tap water. Heads were soaked in 70% ethyl alcohol solution for 24 hours. Arterial and venous systems were injected with pigmented-silicone latex compound (Dow-Corning, Midland, MI) that then hardened overnight. All heads were preserved in a 70% ethyl alcohol solution. Five of 10 heads were dissected to expose the pineal region through the posterior fossa. Sagittal sections were made through this region to study its microsurgical anatomy. The other five heads underwent scanning in the GE High-Speed scanner (General Electric Systems, Milwaukee, WI). Fiducial markers were placed around the occipital=parietal region using a 0-degree angulation and 3-mm thick axial slices for frameless guided (Radionics OTS Frameless Stereotaxy, Radionics Inc., Burlington, MA) localization of the pineal region. Taking advantage of the radiographic characteristics of silicone, we identified the pineal gland by the overlying confluence of siliconeinjected veins that appear as hyperdense structures on computed tomographic (CT) scans (Fig. 1). Computer-assisted cisternal endoscopy (CACE) A straight, rigid, 0-degree, 5-mm Gaab endoscope with a working channel (Codman and Shurtleff Inc.,

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lected as a target (Fig. 2). A localizing wand was used to map the transverse sinus and torcular to plan the keyhole access to the supracerebellar space. The keyhole was placed paramedian within 1 inch of midline with

Fig. 1. Computed tomography scan of a cadaveric head showing hyperdense silicone-injected vessels. Note the confluence of deep veins adjacent to the pineal gland (with permission Mayfield Clinic)

Randolph, MA) and a set of endoscopic surgical instruments were prepared for use. Keyhole access The pre-scanned cadaveric head was placed in a Mayfield head holder (Integra Lifesciences Co., Falmouth, Cornwall, England) and positioned to mimic the semisitting position. Stereotactic fiducials were registered to frameless stereotactic system (Radionics Inc., Burlington, MA). The pineal gland was identified on CT scan in three different planes by the confluence of radio-opaque silicone-injected deep veins into the great vein and se2 Fig. 2. Neural and vascular structures of the pineal region. (A) View through the supracerebellar trajectory. (B) Lateral view of the pineal region after removal of the parieto-occipital lobes and part of the mesencephalon. (C) Sagittal cut through the pineal region after partial removal of the cerebellum. AqS Aqueduct of Sylvius, BVR basal vein of Rosenthal, CA calcarine artery, ICV internal cerebral vein, IOV internal occipital vein, PC posterior commissure, PCA posterior cerebral artery, PChA posterior choroidal artery, PG pineal gland, POA parieto-occipital artery, QP quadrigeminal plate, S splenium, SCA superior cerebellar artery, SS straight sinus, SVV superior vermian vein, Tent tentorium cerebelli, VCMF vein(s) of the cerebellomesencephalic fissure, VG vein of Galen (with permission Mayfield Clinic)

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its upper third overlying the right transverse sinus and the lower two thirds exposing the cerebellum and supracerebellar space.

channel with intermittent irrigation. With direct visualization of the pineal gland, a four-quadrant biopsy was obtained while the deep veins were completely secured.

Endoscopic exposure

Results

After placement of the keyhole, the dura below the transverse sinus was incised and the cerebellum was retracted downward using a ¼ inch Budde-Halo selfretaining retractor blade (Integra Lifesciences Co.) to open the supracerebellar infratentorial space. The rigid endoscope-wand combination was introduced in the supracerebellar space lateral to the arachnoid of the superior cerebellar cistern in midline. Bridging veins from the cerebellum were divided and the cerebellum was further retracted. Continuous real-time update on the position of the endoscope tip and distance from the pineal gland was obtained (Fig. 3). The arachnoid of the superior cerebellar cistern was opened at its junction with the quadrigeminal cistern where the target pineal gland is located. Endoscopic exposure of the pineal gland was correlated with the real-time image of the localizng wand.

In this cadaveric study, the combination of technologies of frameless guided stereotaxy and neuroendoscopy enhanced our ability to navigate the ventriculoscope in narrow spaces such as the posterior fossa cisterns. Compared with transventricular and conventional stereotactic trajectories, the application of CACE in supracerebellar infratentorial trajectory offered the shortest route to the pineal region, allowed easy anatomical orientation, did not necessitate the violation of eloquent neurovascular structures, and provided adequate visibility to the deep veins and arteries. We describe the microsurgical anatomy pertinent to this technique.

Biopsy After the localizing wand was removed, the arachnoid was further dissected from the deep veins and the pineal gland using endoscopic instruments via the working

Microsurgical anatomy The pineal region is located at the junction between the supratentorial and infratentorial compartments posterior to the midbrain in the posterior incisural space. When viewed through the supracerebellar infratentorial approach, the pineal region resembles a cave with walls, roof, floor, and contents. The pineal region comprises cerebrospinal fluid (CSF) cisterns, vascular structures, neural structures, and ventricles – each with relevant anatomy and anatomical relationships. Cerebrospinal fluid cisterns The route to the pineal gland and its ‘‘cave’’ is lined by arachnoid-mater forming cisterns: superior cerebellar and quadrigeminal cisterns. The superior cerebellar cistern is the first cistern encountered in exposure, situated midline between the superior part of the vermis and the arachnoid underlying the straight sinus. This cistern forms a corridor that leads anteriorly to the quadrigeminal cistern and communicates laterally with the subarachnoid space overlying the cerebellar hemispheres. It contains branches of the superior cerebellar artery and superior vermian vein. The quadrigeminal cistern is formed by the arachnoid lining of the pineal cave. Its boundaries and anatomical structures correspond to those of the pineal region.

Fig. 3. Endoscopic view of the pineal region through the supracerebellar-infratentorial trajectory. BVR Basal vein of Rosenthal, ICV internal cerebral vein, VCMF vein(s) of the cerebellomesencephalic fissure, VG vein of Galen, QP quadrigeminal plate, PG pineal gland (with permission Mayfield Clinic)

Vascular structures The venous anatomy of the pineal region is complex – multiple veins converge to drain into the straight sinus

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through the great vein of Galen on top of the pineal gland (Fig. 2A–C). Bridging veins from the cerebellum to tentorial sinuses may be found early in the exposure of the supracerebellar space. Vein(s) of the cerebellomesencephalic fissure is identified posterior to the pineal gland after dissection of the quadrigeminal cistern arachnoid in midline. It drains the superior cerebellar peduncles into the superior vermian vein or directly into vein of Galen. The superior vermian vein receives the cerebellomesencephalic vein and cerebellar veins, and then passes forward above the pineal gland to reach the vein of Galen (Fig. 2C). Internal cerebral veins are paramedian where they exit the velum interpositum of the third ventricle joining to form the vein of Galen in midline. Basal veins of Rosenthal pass laterally from the ambient cistern around the midbrain, enter the quadrigeminal cistern, and drain medially into internal cerebral veins or vein of Galen (Fig. 2B). The internal occipital veins located far lateral and superior in the supracerebellar infratentorial exposure arise in the area of the calcarine and parieto-occipital sulci and pass anteromedially to terminate into vein of Galen (Fig. 2A). Arteries in the pineal region are the posterior cerebral artery and superior cerebellar arteries. These arteries enter the lower anterior part of the quadrigeminal cistern and course below and lateral to the pineal gland. The posterior cerebral artery divides into calcarine and parietooccipital branches (Fig. 2B). The medial posterior choroidal artery on each side enter the quadrigeminal cistern and turn forward passing by the pineal gland to enter the velum interpositum. The superior cerebellar artery passes through the cerebellomesencephalic fissure and branches below the free tentorial edge to supply the tentorial surface of the cerebellum. Neural structures The pineal cave is found after crossing the supracerebellar corridor. This cave has a floor, roof, and anterior and lateral walls formed by different neural structures. The anterior wall consists of the posterior third ventricle and the pineal gland attached to the third ventricular roof at the habenular commissure and posterior commissure (rostral to caudal). The medial pulvinar forms the lateral part of the anterior wall. The quadrigeminal plate forms the lower part of the anterior wall (Fig. 2C). The trochlear nerves exit the brain stem below the inferior colliculi, turning forward around the midbrain and below the pulvinars to enter the ambient cistern. The roof is formed by the splenium of corpus callosum. The lateral

wall is formed by the crus of fornix and the occipital cortex. The floor is formed by the anterior superior part of the cerebellum. Summary The deep veins are located superomedial and the arteries are located inferolateral in the supracerebellar infratentorial trajectory to the pineal gland (Fig. 2A). Study of microsurgical anatomy showed that the supracerebellar infratentorial corridor is a classic trajectory to the pineal region that can be cautiously reapplied to biopsy the pineal region through a new closed biopsy technique. Discussion In our application of CACE in five cadaveric heads, frameless stereotaxy was useful to plan key-hole placement in relation to the midline and transverse sinus, and to provide continuous real-time computer updates on the endoscope’s position in the supracerebellar space. The endoscope provides direct visualization of anatomy, dealing with bridging veins early in exposure and arachnoid dissection of the superior cerebellar cistern and quadrigeminal cistern to expose the deep veins and pineal gland. Management of pineal tumors Tumors in the pineal region have captured the interest of neurosurgeons because of their deep location in the cranium, close relation to the deep venous system, and their great variability in pathology and prognosis. Identification of the exact histological nature makes it possible to tailor therapy according to tumor type and potentially improve the patient’s outcome. Whereas maximum surgical resection may be required in nongerminomatous germ cell tumors (NGGCTs) and benign tumors, adjuvant therapy is more often the more reliable therapeutic method in germ cell tumors. Platinum-based multiagent chemotherapy has improved the outcome in patients with NGGCTs [7]. Radiotherapy is required in all pineal region tumors (except for mature and immature teratomas) with careful consideration given to the dose administered. The extent and dose of radiation is tailored to the specific pathology. Pineoblastomas have a high risk of spinal failure; radiation should be delivered to the craniospinal axis. Germinomas pose a moderately high risk of spinal failure that can only be treated with whole brain irradiation in

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the absence of spinal seeding. In one large series reporting 5-year survival rates of patients with pineal tumors treated by histological diagnosis and adjuvant tumor specific therapy, Schild et al. noted the outcome largely depended on tumor type and radiation dose [23]. While the fore-mentioned examples highlight the necessity for tissue diagnosis to deliver the ultimate management to pineal tumors, they obviously do not settle the long standing debate about the indications for biopsy.

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culoscope has permitted safer access to pineal tumors, biopsy under direct visual observation, possible coagulation of tumor capsule, and the ability to perform therapeutic third ventriculostomy through the same procedure. However, endoscopic biopsy may often be difficult to perform in the absence of large ventricles; it may be more effective in intraventricular tumors and poses difficulty in the manipulation of a flexible ventriculofiberscope.

Computer-assisted cisternal endoscopy (CACE) Biopsy techniques Tumor specimens for diagnosis can be obtained through direct operative approaches, stereotactic biopsy, and endoscopic transventricular approach. Direct surgery is advantageous for obtaining a generous tissue biopsy, being curative for benign tumors, in addition to offering flexibility of a 3-dimensional view of the operative microscope. However, surgery can be associated with possible complications and is not curative in more than 75% of pineal tumors that are locally or metastatically invasive. Frame-based or frameless-guided stereotactic biopsy of the pineal region tumors has emerged as a reliable, less invasive technique. The two primary surgical trajectories to the pineal region for stereotactic biopsy are the posterolateral transparieto-occipital approach and anterolateral transfrontal approach via the anterior limb of the internal capsule. The former trajectory is used for lesions with significant superolateral extension; the latter is more often used for most pineal lesions. The relatively small volume of tumor obtained by stereotactic biopsy challenges the pathologist because of the increased risk of diagnostic error [2, 5]. Furthermore, pineal lesions of mixed cell types are found in 15% of patients and can be misdiagnosed with small biopsies even by experienced neuropathologists [3]. Closed biopsies may also carry risks of intraoperative bleeding from injury to the deep veins or hypervascular tumors or metastatic seeding and tumor implantation along the biopsy tract. Limitations of closed needle biopsy in the pineal region prompted the need for more direct biopsy techniques. Fukushima introduced the concept of endoscopic biopsy of intraventricular tumors under visual control with a flexible ventriculofiberscope [8]. Since then and as a result of the tremendous advances in endoscopic technology, endoscopic biopsy has become more widely used in intraventricular lesions (including pineal tumors) with higher success. The flexible ventri-

The supracerebellar infratentorial approach has been used by most neurosurgeons with a remarkable degree of success in the approach to pineal tumors but had not yet been used as a trajectory during closed biopsy. Use of the supracerebellar infratentorial route for biopsy of the pineal region under direct neuroendoscopic visualization with frameless guided stereotactic guidance enhanced our ability to navigate the ventriculoscope in narrow spaces (e.g., posterior fossa cisterns). Of several recent reports that described the combination of stereotaxy and endoscopy to enhance target localization [4, 10, 19], Rhoten et al. used frameless stereotactic techniques [19] but no one applied this technology outside the ventricular system to biopsy the pineal region. At the beginning of our study, midline placement of the key burr hole required additional drilling of thicker bone and led to the torcular herophilli (which is unnecessary for exposure), mandated arachnoid dissection early in exposure, and necessitated more manipulations of the endoscope. By relocation of the entry point to the paramedian position, we switched to the paramedian supracerebellar trajectory, which allows a more comfortable manipulation of the endoscope and advanced dissection of the superior cerebellar arachnoid closer to the target (at its junction with the quadrigeminal cistern) with real-time computer localization of the target. The paramedian working angle is less steep than the midline angle and offers further access anterolateral to the pineal gland. Use of a localizing wand permits real-time computer updates on the tip position of the endoscope. The wand can be replaced by the instrument registry technology currently available in frameless stereotaxy that allows registration of the rigid endoscope to serve as a localizing wand at the same time. Our initial application of the CACE technique for exposure and biopsy of the pineal region was performed

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in cadaveric brains without pathological conditions. A limitation of our study is that the role of this biopsy technique has yet to be proven in the operating room in patients with pineal tumors, especially without coexisting hydrocephalus. This technique may become a valuable addition to current biopsy techniques. It combines the advantages of being minimally invasive with the potential to yield a direct generous biopsy as in surgery but may decrease the risk of closed intraoperative bleeding. Additionally the technique may help to achieve tumor debulking or even resection.

Technical challenges The view of a novel minimally invasive approach in the cadaver laboratory should not be shortsighted. The CACE approach still awaits the test of real surgery in order to evaluate and overcome the expected difficulties such as the following obstacles: first, the cerebellar retraction in presence of bridging veins in the supracerebellar space; second, arachnoid dissection around major veins in the pineal region, and third, vascular tumors with the risk of bleeding. In its initial application in real surgery, we envision use of a larger craniotomy exposure for CACE in which to introduce the endoscope early on and allow adequate vision and coagulation of bridging veins. Arachnoid dissection deep in exposure can be performed using a rigid endoscope, which can reach deep and anterolateral to the major veins of the pineal region with more detailed anatomical view. The larger craniotomy will eventually be tailored to a ‘key-hole’ exposure once experience and comfort accumulate with CACE. The modern technology in neuroendoscopy has offered technical flexibility in manipulation, dissection and thermocoagulation hemostasis through a multicompartment working channel. Yet, the surgical microscope can intervene when bleeding becomes a challenging task in minimally invasive surgery.

Conclusions Computer-assisted cisternal endoscopy may be used to approach lesions outside the cereberal ventricular system to obtain a biopsy or perform debulking. Continuous computer update on the endoscope position allows its safe navigation in narrow spaces like the cerebrospinal fluid cistern. This technique can be applied to biopsy pineal tumors in the absence of hydrocephalus and its success will await future surgical trials.

Acknowledgements The authors thank Norberto Andaluz, M.D., Khaled M. Abdel Aziz, M.D., Ph.D., and Salah K. Hemida, M.D., Ph.D. for cadaveric preparation and technical assistance.

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