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Endoneurosurgical Resection of Intraventricular and Intraparenchymal Lesions Using the Port Technique Nancy McLaughlin1, Daniel M. Prevedello2, Johnathan Engh 3, Daniel F. Kelly1, Amin B. Kassam1,4

Key words 䡲 ●●● Abbreviations and Acronyms CSF: Cerebrospinal fluid ICP: Intracranial pressure MRI: Magnetic resonance imaging From the 1Neuroscience Institute & Brain Tumor Center, John Wayne Cancer Institute at Saint John’s Health Center, Santa Monica, California, USA; 2Department of Neurological Surgery, The Ohio State University, Columbus, Ohio, USA; 3Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA; and 4Department of Surgery, Division of Neurosurgery, University of Ottawa, Ottawa, Ontario, Canada To whom correspondence should be addressed: Amin B. Kassam, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2012). http://dx.doi.org/10.1016/j.wneu.2012.02.022 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter © 2012 Published by Elsevier Inc.

INTRODUCTION Deep-seated intracranial lesions, including intraventricular and intraparenchymal pathologies, have traditionally been removed under direct microscopic visualization. More recently, the use of intraoperative neuronavigation has enabled the surgeon to precisely plan the craniotomy in order to reach lesions while traversing the least possible amount of normal nervous tissue. However, in order to access such deepseated lesions, transcortical approaches require a corticectomy and some degree of dissection of the overlying white matter. Depending on the extent of the corticectomy and white matter fascicular dissection, the use of brain retraction is often required to maintain the corridor created to reach the lesion. This is essential for optimal visualization throughout the intracranial procedure and enables bimanual dissection by freeing both hands. Unfortunately, the occurrence of brain contusion or infarctions after the use of brain retractors

is not uncommon. The incidence of brain retraction injury varies from 5% to 10%, of which some potentially may be manifest clinically (1, 10, 21, 24). Patrick Kelly developed a less disruptive way to reach deep-seated lesions in the brain by using a sequence of cylinders to dilate the brain parenchyma (12-14). There is a need of a 2-cm minimum cylinder diameter to allow binocular three-dimensional visualization when the microscope is utilized in this setting. The authors have adapted this technique allowing resection of deep-seated lesions through a smaller transparent conduit (port) using endoscopic visualization. This technique ensures that the initial diameter of the corticectomy and white fiber tract dissection remain stable throughout the intervention. Furthermore, white matter damage is minimized as the wedged-tip dilator separates the fascicles during the cannulation. The transparent port allows maintenance of a safe corridor, protecting the cortex and surrounding white matter against instrument manipulation throughout the case. It prevents inadvertent expansion of the corticectomy and/or fasciculotomy. Most importantly, this conduit enables homogeneous pressure on the surrounding tissue with dynamic adjustments of its position. Initially we developed experience with intraventricular lesions such as colloid cysts, and subsequently started to use the techniquetodrainintraparenchymalhematomas(9, 11). Recently we reported our experience on this method for resection of intraparenchymal tumors discussing its advantages and limitations compared to other techniques (11).

OPERATIVE TECHNIQUE—GENERALITIES OF THE VENTRICULOPORT AND THE BRAINPORT TECHNIQUES Perioperative Considerations and Anesthesia Patients undergo an image-guided contrast-enhanced magnetic resonance imag-

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ing (MRI) with thin axial cuts. If an MRI is contraindicated, a CT scan with fine cuts may be done instead. For subcortical lesions in proximity to critical white matter fascicles, white matter mapping with highdefinition fiber tracking imaging may be an important complementary investigation (8). Surgery is performed under general endotracheal anesthesia. Antibiotic, mannitol, corticosteroids, and antiseizure drugs (phenytoin or levetiracetam) are systematically used perioperatively. Mild hyperventilation serves to maintain a PCO2 around 30 mm Hg until the lesion is completely removed. Normotension is favored throughout the case. Except for the patients with a cerebellar tumor, patients are positioned supine in a three-point Mayfield headholder. The head position is adapted to the specific tumor location but ensures that the head is positioned above the heart level. All procedures are performed with intraoperative frameless image guidance with either scalp fiducials or mask registration (Stryker, Inc.).

Trajectory Planning, Craniotomy, Corticectomy The trajectory and site of the craniotomy is determined using the neuronavigation. For lesions within the lateral ventricle, the tumor laterality determined the side of the approach. Third ventricular lesions were approached from the side of the most dilated lateral ventricle. Specifically, the trajectory was selected to avoid injury to the internal capsule and the head of the caudate nucleus. The craniotomy was located anterior to the coronal suture. The right side was always used in symmetric lateral ventricles. For intraparenchymal lesions, the trajectory is planned using anatomic landmarks. For obvious reasons, a trajectory should never be planned through eloquent cortex such as the motor strip, visual cortex, superior temporal gyrus, and inferior frontal gyrus. When possible, the dominant parietal lobe

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should also be avoided. Occipital trajectories were more than 3 cm lateral to the midline. Cerebellar trajectories were also lateral to the midline (11). The craniotomy is centered on the entry point of the best trajectory and measures between 2.5 and 3 cm. A smaller craniotomy can limit the ability for port angulations as it ends up touching the bony edge. Once the dura is opened in a cruciate fashion, the superficial sulci and cortical vascular anatomy are inspected. In some instances, the initial optimal trajectory must be readjusted given the presence of major draining veins blocking access to the desired sulci. Once the optimal trajectory is determined, either transgyral or transsulcal, a corticectomy measuring 5 to 6 mm is performed over a noneloquent cortex.

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Port Preparation and Cannulation After performing the corticectomy either on the gyrus or through the depth of a sulcus, the length of the port must be adjusted for each case (Figure 1). For intraventricular lesions, the distance from the inner table to the ependymal surface should be measured.

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For intraparenchymal masses, the distance from the inner table to the deepest portion of the tumor is noted. In both situations, an additional segment must be planned to allow some extension of the port above the cortical mantle during resection. The tailored port is mounted on the wedged-tip dilator. The new port system allows the neuronavigation wand to fit in its central orifice, enabling cannulation under direct navigation. This allows the surgeon to adjust the trajectory’s direction as the dilator and port approach the target. The cannulation with the dilator is typically targeted just passed the ependymal surface for ventricular lesions. Once in adequate position, the neuronavigation probe is withdrawn and cerebrospinal fluid pours out. CSF is further suctioned, creating an air environment for surgery to proceed. For intraparenchymal lesions, cannulation should aim the deepest portion of the lesion (if resistance is not encountered), allowing the mass to deliver itself through the channel. In both circumstances, once the port is in adequate position, it should be secured in order to prevent its migration during the procedure. The rest of the intervention proceeds entirely under

Figure 1. (A) Verifying the trajectory with the neuronavigation after exposing a transsulcal route. (B) Cannulation of the port mounted on the dilator under direct navigation. (C) Removal of the dilator. (D) Installation of the endoscope holder, proceeding to bimanual tumor removal under endoscopic visualization.

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direct endoscopic visualization. Initially, the 0-degree endoscope (Storz) is attached to an endoscopic holder, which allows, dynamic movement in any plane during the procedure. The endoscope should be kept at 12 o’clock during the procedure because the other instruments occupy the rest of the space within the port.

Lesion Removal Specific details relevant to intraventricular lesions and intraparenchymal tumor removal will be discussed through two illustrative cases. Illustrative Case 1: Colloid Cyst Approached via the Ventriculoport. A 31-year-old woman in previous good health was referred for recent onset of increasingly frequent headaches with bouts of intermittent confusion, gait difficulty, and vision alteration (Figures 2 and 3). A brain MRI showed a 7- ⫻ 8-mm lesion in the anterior part of the third ventricle. This cystic mass was situated more toward the left. Although the ventricles remained of small size, the left was slightly larger than the right. Her neurologic examination was normal. The patient was recommended removal of the suspected colloid cyst through a microscope-assisted endoscopic port surgery. Surgery was performed through a left frontal minicraniotomy given the larger size of the left ventricle. Under direct image guidance, the cannulation proceeded via a transsulcal opening. After removal of the cannula, CSF poured out and the rest of the procedure proceeded in an air medium. A cuff of ependyma was seen and cut. Anatomic landmarks inside the lateral ventricle were identified. In this case, the caudate was the first structure identified given its bulge into the left lateral ventricle. A septostomy was performed to allow CSF egress from the contralateral ventricle. The choroid plexus and venous structures were next identified. The choroid plexus was followed anteriorly to where it turns at the foramen of Monroe. The fornix was viewed medially and appeared of small size. In addition to the neuronavigation, intraoperative recognition of the thalamostriate vein, located posterolaterally, and the septal vein, located anteromedially at the foramen, confirmed adequate location and laterality. In this case, the venous angle completely encircled the lesion, and a transforaminal approach was not deemed safe. The cyst was

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lesion to the most superficial components. As the deepest part of the tumor is removed, the conduit is delicately withdrawn, allowing a more superficial component to deliver itself within the port. Throughout, tumor removal care is taken not to suction the surrounding edematous white matter as this may create venous bleeding. Hemostasis is performed using a modified bipolar for arterial bleeding and tamponade with hemostatic agents and warm saline irrigation for venous bleeding.

Figure 2. (A) Identification of key structures, including the head of the caudate nucleus and its vein, choroid plexus (*). (B) Exposure of the cyst (**) through a transchoroidal route. (C) Resection of the cyst’s capsule. (D) Irrigation within the third ventricle via a ventriculostomy catheter.

approached through a transchoroidal route. After its puncture, the cyst collapsed and its attachment to the choroid plexus was visualized and transected. The capsule of the cyst was resected except for a small part of the wall posteriorly stuck to the internal cerebral vein. The postoperative MRI confirmed resection of the colloid cyst and the patient had an uneventful postoperative case.

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Illustrative Case 2: Brain Metastasis Approached via the Brainport. A 56-year-old woman was referred for a newly diagnosed right frontal solitary brain lesion (Figures 4 and 5). She had been diagnosed with a left thumb melanoma treated with partial amputation of the first digit and sentinel lymph node dissection that was negative. No adjuvant therapy was administered. Two years later, she presented lymph node recurrence and was diagnosed with lung and liver metastases. She underwent biochemotherapy. Five years out of her initial diagnosis, her most recent MRI showed a right frontal intraaxial mass measuring 25 ⫻ 20 mm with significant surrounding edema. The lesion is anterior to the motor strip and is approximately 10 mm from the cortical surface. The patient was proposed tumor resection using the microscope-assisted endoscopic brainport technique. After verifying the tra-

jectory with the neuronavigation, the sulcus overlying the lesion was dissected and opened on 5 mm under microscopic visualization. Using the surgical navigation, the brainport mounted on the dilator was cannulated into the lesion to a depth of approximately 4 cm. The cannula was removed and the hemorrhagic tumor was seen bulging in the conduit. Once the dilator is removed, tumor initially fills up the cavity of the port. This part is removed using initially a tumor grasper in order to obtain tissue for pathology assessment. Afterwards, the double suction technique is used. Initially, a suction is used to provide countertraction on the tumor while the other suction is aspirating. After debulking the central component, one of the suctions may be used to retract the port in various directions, enabling more tumor to deliver itself in the conduit and subsequent debulking to proceed. Microdissection is performed with the adapted microinstruments using both hands. Fibrotic tumors may be addressed using adapted microscissors or using a modified endoscopic ultrasonic aspirator. More recently, we have also used a sidecutting aspiration device (NICO Myriad device; NICO Corporation, Indianapolis, Indiana, USA) through the port. Tumor removal must proceed from the deepest parts of the

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Removal of the Port and Closure After removal of the ventricular or intraparenchymal lesion, a ventriculostomy catheter is placed under direct visualization at the bottom of the cavity. After the surgical cavity is irrigated and hemostasis is impeccable, the port is removed. The white matter can be seen resuming its normal position. The site of cannulation is covered by a piece of Duragen or Helistat (Integra Life Sciences, Plainsboro, New Jersey, USA). The bone flap and skin are closed in a standard fashion.

DISCUSSION Brain Retraction With the improvement of microneurosurgical techniques, brain retraction became essential for adequate exposure during many intracranial interventions. The introduction of self-retaining retractors after handheld retractors enabled surgeons to pursue bimanual microsurgical dissection (6). It was described that the self-retaining brain retractors would apply pressure to the underlying brain surface under the surgeon’s control as he or she would adapt the pressure in response to the feel of the tissue resistance (22). However, numerous studies have assessed the impact of brain retraction from the viewpoint of morphology, cerebral blood flow, electrophysiology, and metabolism (1, 10, 21). Brain damage seems to be caused by focal pressure of the retractor blade, which induces local deformation of the brain tissue with resultant ischemia and also direct injury such as cutting and tearing parenchyma. Brain injury secondary to retraction occurs in approximately 10% of major skull base cases and 5% of intraaxial tumor and intracranial aneurysm

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Figure 3. (A) Preoperative magnetic resonance imaging (MRI) showing the colloid cyst and slightly larger left lateral ventricle. (B) Postoperative MRI

surgeries (1). In some instances, such injury may be clinically significant (10, 21, 24). Some reports have proposed that there may be a range of safer pressure or overall retraction technique (10). Factors that have been related to less retraction injury are retractor pressure of 30 mm Hg or less, frequent repositioning of each retractor, and use of multiple retractors to decrease the pressure exerted by each individual retractor (1, 10, 21, 24). In addition, different varieties of brain spatulas have been proposed, each presenting specific features (6). Despite these precautions, brain injury due to retraction still occurs (1, 17).

Evolution of the Concept of Intraaxial Brain Surgery Through a Sheath Parallel to the popularized use of self-retained brain blades, the concept of a tubular retraction system was introduced in the late 1980s. Kelly et al. proposed a hollow cylinder 20 or 30 mm in diameter used to resect

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confirming resection of the colloid cyst.

intraparenchymal tumors under microscopic visualization. The tubular retraction system provided a route for stereotactic removal of deep-seated intracranial lesions (12-14). In 2000, Nishihara described the use of a transparent sheath (inner diameter: 6 mm, outer diameter: 8 mm) for endoscopic evacuation of intracerebral hematoma (19). The sheath accommodated a 2.7-mm endoscope and a 2.5-mm suction tube. Hematoma removal was performed with one hand. The authors stated that the use of a transparent sheath allowed appreciation of the border between the hematoma and the brain, to redirect the tip of the sheath to achieve complete hematoma drainage and to examine the hematoma cavity. Barlas introduced in 2004 a plastic cylindrical retractor (inner diameter: 12 mm, outer diameter: 14 mm) mounted on a dilator with a conical tip (2). The dilator was attached to a stereotactic arc. A transfrontal–transforaminal trajectory was used to gain access to colloid cysts. The authors

supported that the cylindrical retractor enabled adequate surgical exposure under microscopic visualization with a minimal retraction force on the surrounding tissue. The following year, Chen used a stainlesssteel sheath (inner diameter: 8 mm; outer diameter: 10 mm) to guide the endoscope during the evacuation of deep-seated hematomas (5). This sheath accommodated an endoscope (4 mm) and a suction tube (2.5 mm). The authors emphasized the ease of hematoma evacuation in an air medium in comparison to a fluid medium, the former ensuring a much clearer image. Ogura rolled a polyester film into a cylinder measuring 8 mm and mounted on a holding needle with a wedged tip (20). Once inserted to the desired depth, the needle is removed and the cylinder may be expanded up to 2 cm in diameter. The transcylinder approach enabled microsurgical removal of intraaxial tumors under microscopic visualization. Interestingly, the retracting pressure around the cylinder was measured ad-

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Figure 4. (A) As tumor resection proceeds, tumor fills up the cavity of the port. (B) Gentle peeling of the tumor from the edematous underlying white matter using double suction technique. (C) During decannulation, hemostasis is made along the trajectory of the port and at the end the surrounding cortex is also inspected. (D) Demonstration of the minimal transsulcal route required.

jacent to the cylinder using a Camino and was always below 10 mm Hg. Accordingly, the retraction force produced by the cylinder seemed to be distributed more equally and to dissipate along the whole surface of the surgical route (20). In 2009, Nakano described using a transparent sheath (outer diameter: 8 mm) for biopsy of intraparenchymal lesions (18). The sheath was inserted into the target stereotactically and biopsy specimen obtained under direct visualization. In one case, frameless neuronavigation was combined to endoscope. The sheath was inserted with real-time monitoring using neuronavigation (18). More recently, Warran proposed an expandable cannula system for endoscopic evacuation of intraparenchymal hemorrhages (23). The system consists of two metal blades that are covered with a plastic sheath. As the blades open, a rectangular tunnel measuring 16 ⫻ 5 mm is formed within the parenchyma. The authors did not find any significant increase in intracranial pressure (ICP) measurements before and during cannulation. No accurate ICP reading was available when the cannula was open given the rapid drainage of the hematoma that caused a drop in the ICP (23).

In summary, these sheaths (either cylindrical or rectangular) protect the brain from accidental injuries caused by instruments being passed in and out of the route. They also prevent the inadvertent increase in size of the corticectomy and white matter fasciculotomy throughout surgical manipulation. Although these sheaths seemingly allow instruments to move independently to the camera, little freedom of movement is available in most of them. The instrument often remains in the same line of sight as the endoscope, as has been noted for endoscopic sheaths incorporating one or two working channels (4, 16). In most of these studies using endoscopic visualization, the size of the sheath only accommodates the endoscope and an additional instrument such as the suction. Although some authors might find this satisfactory for hematoma evacuation, bimanual surgery is a prerequisite for tumor removal. As such, some authors have proposed incorporating a second adjacent portal to counterbalance the lack of bimanual dissection in colloid cyst (3, 15). In our opinion, microsurgical and endoneurosurgical principles should not be sacrificed for the sake of noninvasiveness.

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Evolution of the Ventriculoport and Brainport Technique To operate bimanually with the microscope, the tubular retractors developed by Kelly and more recently by Oruga et al. required a larger diameter conduit since the microscope was used to deliver a cone of light as it tapers progressively from the source to the target (12-14, 20). Because the endoscope affords a panoramic view via an inverted cone of light and allows dynamic magnification, we postulated that it could be the sole source of visualization during intracranial surgery performed through a sheath. It was therefore possible to decrease the size of the conduit but without sacrificing the ability to perform bimanual surgery. As noted in other techniques, we conceived the distal tip of our dilator in a wedged shape to ensure that it dissects through the white fiber fascicles, recognizing that a small amount of fibers will inevitably be transected without the need for multiple progressive cylinder diameters. Although smaller-caliber endoscopes have been tried, in our opinion the 4-mm rigid endoscope has afforded the best intraoperative images. Our experience with endoscopic port surgery for intraventricular lesions has been published in 2005 and 2010 and for intraparenchymal lesions in 2009 (7, 9, 11). As for all new techniques, a learning curve exists and is potentially less steep for surgeons skilled in endoscopic techniques and used to working through small corridors such as keyhole and endonasal approaches. Interestingly, when this technique is performed by two surgeons skilled in endoscopic surgery, the endoscope may be handheld throughout the surgery, enabling a dynamic view with up and close views in the same manner as for endonasal endoscopic surgery. In comparison to the other procedures performed through a sheath, the port offers numerous advantages. Given the wedged configuration of the distal tip of the dilator, cannulation proceeds mostly by dilating the white matter fibers. The cannula is penetrated gently, allowing the brain to adapt. Importantly, the fact the ICP does not increase during the insertion of large cylindrical retractors is possibly because it works as an infinite number of small retractors organized in a circular fashion. The port redistributes the pressure more equally in the surrounding tissue. The cylindrical config-

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Figure 5. (A) Preoperative magnetic resonance imaging showing the right frontal intraaxial mass spontaneously hyperintense on T1-weighted sequences. (B) Postoperative computed tomography scan (bone windows)

uration of the port also seems advantageous in comparison to the flat rectangular retractors, which may cause direct cutting and/or tearing trauma to the underlying brain tissue. The port may accommodate a 4-mm rigid endoscope and two instruments. Therefore, tumor removal may proceed with a bimanual microsurgical technique. Importantly, this conduit allows removal of lesions larger than the diameter of the port since the tumor is removed piece by piece in a circular fashion from deep to superficial. Because the tumor feeds itself into the port given the direction of less resistance and since suction and dissection technique help bring the tumor within the port cavity, minimal manipulation is made on the white matter surrounding the lesion. The cylin-

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demonstrating the tailored craniotomy and MRI confirming complete tumor resection.

drical form of the port also enables less traumatic manipulation in the white matter and cortex dissected to gain access to the target. With the advent of new technology, port surgery has been improved. The introduction of high-definition fiber tracking guidance for endoscopic port surgery has enabled adjustment of the cannulation entry point and as well as the trajectory thanks to detailed assessment of subcortical anatomy (8). New instruments have been developed for the removal of more fibrotic lesions. Although the double suction and piecemeal removal techniques have proven to be safe and effective through the port, they may prolong operative time for fibrous tumors. The NICO Myriad device is a multifunc-

tional bayoneted instrument that allows the user to direct controlled and precise tissue shaving, gross tissue debulking and blunt dissection. We have found the device’s multifunctional ability to reduce the number of instruments needed in the port procedure and secondarily preclude the need for multiple instrument insertions into the surgical field.

CONCLUSION AND FUTURE DIRECTIONS In experienced hands, the port technique is an appealing surgical option for the removal of intraventricular and intraparenchymal lesions. The impact of the port from the viewpoint of brain morphology, cere-

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bral blood flow, and metabolism still needs to be assessed. Patient outcome and qualityof-life assessments are also needed to determine potential benefits of this technique in comparison to more traditional approaches. The adjunct of new technologies such as high-definition fiber tracking and new instrumentation will inevitably fuel the progress of the endoscopic port surgery.

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an analysis of causes and patient outcomes. J Neurosurg 101:600-606, 2004. 18. Nakano T, Ohkuma H, Asano K, Ogasawara Y: Endoscopic treatment for deep-seated or multiple intraparenchymal tumors: technical note. Minim Invasive Neurosurg 52:49-52, 2009. 19. Nishihara T, Teraoka A, Morita A, Ueki K, Takai K, Kirino T: A transparent sheath for endoscopic surgery and its application in surgical evacuation of spontaneous intracerebral hematomas. Technical note. J Neurosurg 92:1053-1055, 2000. 20. Ogura K, Tachibana E, Aoshima C, Sumitomo M: New microsurgical technique for intraparenchymal lesions of the brain: transcylinder approach. Acta Neurochir (Wien) 148:779-785; discussion 785, 2006. 21. Rosenorn J, Diemer N: The risk of cerebral damage during graded brain retractor pressure in the rat. J Neurosurg 63:608-611, 1985.

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22. Sugita K, Kobayashi S, Takemae T, Matsuo K, Yokoo A: Direct retraction method in aneurysm surgery. Technical note. J Neurosurg 53:417-419, 1980.

12. Kelly PJ: Technology in the resection of gliomas and the definition of madness. J Neurosurg 101:284-286; discussion 286, 2004.

23. Waran V, Vairavan N, Sia SF, Abdullah B: A new expandable cannula system for endoscopic evacuation of intraparenchymal hemorrhages. J Neurosurg 111:1127-1130, 2009.

13. Kelly PJ, Goerss SJ, Kall BA: The stereotaxic retractor in computer-assisted stereotaxic microsurgery. Technical note. J Neurosurg 69:301-306, 1988. 14. Kelly PJ, Kall BA, Goerss S, Earnest F 4th: Computerassisted stereotaxic laser resection of intra-axial brain neoplasms. J Neurosurg 64:427-439, 1986. 15. King WA, Ullman JS, Frazee JG, Post KD, Bergsneider M: Endoscopic resection of colloid cysts: surgical considerations using the rigid endoscope. Neurosurgery 44:1103-1109; discussion 1109-1111, 1999.

24. Yokoh A, Sugita K, Kobayashi S: Intermittent versus continuous brain retraction. An experimental study. J Neurosurg 58:918-923, 1983.

Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 16 August 2011; accepted 02 February 2012 Citation: World Neurosurg. (2012). http://dx.doi.org/10.1016/j.wneu.2012.02.022

16. Kunwar S: Endoscopic adjuncts to intraventricular surgery. Neurosurg Clin N Am 14:547-557, 2003.

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17. McLaughlin N, Bojanowski MW: Early surgery-related complications after aneurysm clip placement:

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www.WORLDNEUROSURGERY.org

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349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 AQ: 5 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406