Original Article a Virtual Reality Model of the Clivus and Surgical Simulation Via Transoral Or Transnasal Route

Int J Clin Exp Med 2014;7(10):3270-3279 www.ijcem.com /ISSN:1940-5901/IJCEM0001972

Original Article A virtual reality model of the clivus and surgical simulation via transoral or transnasal route

Shou-Sen Wang*, Jun-Feng Li*, Shang-Ming Zhang, Jun-Jie Jing, Liang Xue

Department of Neurosurgery, Fuzhou General Hospital, Fujian Medical University,156 Xihuanbei Road, Fuzhou 350025, China. *Equal contributors. Received August 19, 2014; Accepted September 20, 2014; Epub October 15, 2014; Published October 30, 2014

Abstract: Background: Neurosurgery in areas with restricted space and complicated anatomy can be greatly aided by the virtual reality (VR) technique. The clivus represents one of such challenging surgical areas, but its VR has not been established. The present study aimed to document a VR model of clival anatomy that may be useful in clival surgery. Methods: High resolution CT angiography and MRI were used. The study included a total of 20 patients who did not have any obvious abnormalities detected in the oral, nasal, and clival areas. The images were fused with a Dextroscope. Results: In the VR model, the key structures such as the clival bone, basilar artery, brainstem, pituitary gland, and paranasal sinuses were clearly observed. The morphology of the clivus and its spatial relationships with the neighboring structures were also illustrated. Visualization of the clival model can be made flexible from various planes, angles, or orientations. In addition, surgical access to the clivus via the transoral route or transnasal route was simulated in detail. Conclusion: The simulation of the VR model offers a straightforward, three-dimensional, interactive understanding of the size and shape of the clivus, and its relationships with the surrounding blood vessels and bones. It also demonstrates simulated operational procedures such as opening the surgical window, measuring the exposure distance and angles, and determining the critical boundaries in relation to key structures such as the brainstem and arteries. Digitalized VR modeling appears to be helpful for understanding the anatomy of the clivus and its surgical approaches.

Keywords: Clivus, digitalized anatomical model, transnasal, transoral, surgical simulation

Background The clivus is a rather challenging surgical site due to very restricted surgical space and being Neurosurgery in areas with restricted space surrounded by several vital structures [6]. The and complicated anatomy tends to be associ- development of clival surgery guided by VR ated with higher morbidity. Preoperative plan- would be an essential addition to neurosurgery ning and surgical practice are the key to obtain- education and training [7]. The clival VR model ing better surgical outcomes. In the old days would enable simulation of the surgical opera- when only cadavers were available, the sur- tion and provide preoperative measurement of geons were left with very limited chances to the anatomical structures. It also represents optimize or improve the surgical skills. However, unlimited training opportunities for new sur- the advent of virtual reality (VR) opened up pos- geons who wish to become very skillful in man- sibilities for aiding surgical access to challeng- aging the area. ing sites [1-4]. VR represents an innovative paradigm in surgical simulation [1, 5]. It enables Surgical approaches to the clivus are either via the anatomical environment to be recreated in the transnasal route or transoral route in order a virtual space without the requirement of to deal with clival pathologies including mucous physical models. VR aids in surgical planning cyst, chordoma, chondrosarcoma, craniopha- and preoperative evaluation, and has contrib- ryngioma, meningioma, and pituitary adenoma uted to reforming surgical paradigms. The doc- [6, 8-10]. The clivus is located in the midline umentation of VR aided neurosurgery is a very area of the skull base. It is part of the cranium, important step to solidify the neurosurgical formed by the basilar part of the occipital bone education and planning. and the corpus ossis sphenoidalis. The clivus Clival virtual reality surgical simulation

Figure 1. Raw clival images from (A) CTA and (B) MRI. sits between the anterior foramen magnum of guide in preoperative education/evaluation the occipital bone and the posterior clinoid pro- and surgical planning during the management cess, and slopes obliquely backward at an of clival pathologies. angle of approximately 45 degrees. The dorsal part of the clivus is the dorsum sella, and it is Materials and methods bordered ventrally by the anterior foramen Subjects magnum of the occipital bone. Lateral to the clivus is the foramen lacerum, petrooccipital This study was approved by the Institutional fissure, jugular foramen, and internal aperture Review Board of Fuzhou General Hospital, of the hypoglossal canal. The clivus is posi- Fujian Medical University. All patients included tioned in a very central site of the skull base, in this report were admitted to Fuzhou General and it is near several vital structures including Hospital between May 2010 and January 2012 the brainstem, internal carotid artery, fifth, and were diagnosed with spontaneous sub- sixth, and seventh cranial nerves, cavernous arachnoid hemorrhage, but did not have pathol- sinus, hypophysis, and hypothalamus. The sur- ogies identified in the skull base. These patients rounding important structures allow only very underwent brain CT and MRI [13]. The study limited surgical exposure of the clivus. included 20 patients, 12 males and 8 females. Patient age ranged from 25 to 70 years. CT The goal of the present study is to document a angiography (CTA) confirmed that these pa- VR model of clival anatomy that may be useful tients had cerebral anterior circulation aneu- in clival surgery [3]. In addition, measurements rysms, and all underwent the clipping surgery between key landmarks would be taken to bet- successfully. On CT scans, no obvious abnor- ter define the local anatomy, the coverage, and malities were found in the oral, nasal, or clival the orientation for safe bony removal during areas. Consent to allow use of the imaging data surgery. To this end, the present study took was obtained from the participating patients. advantage of high resolution medical imaging to simulate the clival anatomical environment Image acquisition and then create a clival VR model with the digitalized information available [11, 12]. Moreover, Computed tomography angiography was per- we aimed to simulate in detail the surgical formed using a 64-slice spiral CT scanner access to the clivus via the transoral or trans- (Discovery Ultra, GE). The rotator time was 0.5 nasal route. The clival VR model may serve as a s/rotation with 120 kVp and 200 mAs, the slice

3271 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation

Figure 2. VR model established from CTA and MRI. A. An overview of the digitalized clival VR model. The cranial bone is in amber; the basilar artery in red, the brainstem in green, the sphenoidal sinuses in blue, the pituitary gland in yellow, and the ethmoid sinus in spring green; B. A side view of the clivus and its spatial relationships with the surrounding structures. The clival bone is in amber, the brainstem in green, the basilar artery in red, the pituitary gland in purple, and the sphenoidal sinuses in blue; C. A top down view; D. A bottom up view. thickness was 0.625 mm, the slice interval was the field of view was 250 mm×250 mm, and the 0.625 mm, the field of view was 240 mm×240 matrix size was 512×512. T1-weighted imaging mm, and the matrix size was 512×512. The used a repetition time (TR) of 1900 ms and an contrast media, iohexol (Omnipaque), was echo time (TE) of 2.52 ms. T2-weighted imaging injected at the dose of 2 ml/kg via the cubital used a TR of 3200 ms and TE of 403 ms. All the vein with an infusion rate of 3.5 ml/s. Magnetic image sequence data were stored on a CD-ROM resonance imaging was performed using a 3.0 in DICOM format. T MRI scanner (Trio Tim, SIE Company) with Co-registration of MR and CT datasets MPRAGE (magnetization prepared rapid acquisition gradient echo) sequence with coverage The CTA and MRI datasets were co-registered of the head region in the coronal plane. The using a 3-D workstation with a Dextroscope slice thickness was 1.0 mm with no interval, (Volume Interactions/Bracco, Singapore) [14,

3272 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation

Table 1. Measurement between the anterior nasal spine and the clivus _ X ±s Distance between the anterior nasal spine and the sellar floor (mm) 78.8±3.1 The angle formed by the nasal base and the line connecting the anterior nasal spine and the sellar floor (°) 31.7±0.9 Distance between the anterior nasal spine and the dorsum sellae (mm) 83.6±4.3 The angle formed by the nasal base and the line connecting the anterior nasal spine and the dorsum sellae (°) 33.0±1.8 Distance between the anterior nasal spine and the clival recess (mm) 81.7±5.9 The angle formed by the nasal base and the line connecting the anterior nasal spine and the clival recess (°) 31.6±2.3

15]. This is a system that enables integration of using a Dextroscope. As demonstrated in Fi- tomographic images from CT and MRI into true gure 2, the position of the key structures such 3-D volumetric objects that can be viewed ste- as the clival bone, basilar artery, brainstem, reoscopically. Skin fiducials visible in both data pituitary gland, and paranasal sinuses were sets were specified as landmarks. The co-regis- clearly observed. The morphology of the struc- tration was performed with least-squares error ture and its spatial relationship to the neighbor- minimization. Both manual and automatic ing structures were also illustrated. Visualization adjustment was made to ensure the accuracy of the clival model can be made flexible from of the co-registered 3-D model with the image various planes, angles, or orientations. The raw contrast and coverage optimized. CTA mainly states can be recovered without any limits. re-established the cranium and blood vessels while MRI reconstructed the soft tissues includ- Measurement in the clival model ing the pituitary gland and the brainstem. The clival VR model indicates that on the mid- Important anatomical structures such as the sagittal section, the full length of the clivus is sphenoidal sinus, intracranial arteries, pituitary 30.6-51.2 mm, with the average length being gland, brainstem, etc. were labeled in the VR 41.7±2.9 mm. Frontal to the superior clivus is model with digitalized information available the hypophyseal fossa and the sphenoidal (Figures 1 and 2). sinuses. Frontal to the inferior clivus is attach- Visualization and simulation ment of the soft tissue of the posterior pharyn- geal wall. Lateral to the clivus is the cavernous In the co-registered clival VR system, various sinus and the petrous part of the temporal functions were available for detailed explora- bone with the internal carotid artery, abducens tion and visualization. The shape, size, and ori- nerve, and trigeminal nerve passing through. entation of the structures can be studied read- The distances were measured between the ily while measurement and marking can be anterior nasal spine and the structures around made easily. Simulation of the conventional the clivus, and are summarized in Table 1. transnasal and transoral routes to the clivus The distribution of the sphenoidal sinuses var- was also demonstrated. The simulation includ- ies among individuals. In some individuals, the ed the procedures involved in opening the clival sphenoidal sinuses extend as far as adjacent to bone window, viewing from different angles, the dorsum, to the pterygoid plate and the and measuring the safety width of the window. greater wing of the sphenoid bone, and even to The images were stored with the data collect- the basilar part of the occipital bone. The pos- ed. Statistical analysis using SSPS 13.0 soft- terior and inferior walls of the sphenoidal sinus- ware was performed to obtain the descriptive es are anatomically interconnected with the statistics in Tables 1 and 2. clivus; the posterior wall directly constitutes a Results part of the superior clivus while the inferior wall is linked with it. The carotid artery ascends per- Overview of the clival VR model pendicularly to the cranium and then becomes the internal carotid artery. The artery then turns The raw images of the clival region from CTA medioanteriorly, proceeds horizontally, passes and MRI are shown in Figure 1. After image through the foramen lacerum, turns upwards fusion, the clival VR model was established after the passage, and then enters the cavern-

3273 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation

Figure 3. Surgical simulation via the transnasal route to the clivus. A. In the transnasal surgery, the middle and inferior nasal concha are removed with the nasal septum preserved. The anterior wall and the opening of the sphenoidal sinuses are preserved; B. The pituitary gland and the internal carotid are exposed after the removal of the anterior, lateral wall of the sphenoid sinus and the bone of the sellar floor; C. The brainstem and basilar arteries behind the clivus are exposed after the further removal of the inferior wall of the sphenoid and the posterior bone; D. The coverage of the opened window for the clival surgery is shown after the further removal of the inferior clival bone. The cranium is in amber, the clival bone in yellow, the sphenoidal sinuses in blue, the pituitary gland in purple, the brainstem in spring green, the internal carotid and the basilar arteries in red. ous sinus. This study shows that the shortest approximately 1 cm. It is bordered anteriorally distance between the bilateral internal carotid by the corpus ossis sphenoidalis, inferior ptery- arteries is 18.8±1.9 mm, and the two arteries goid process, and the greater wing of the sphe- at the level of the sellar floor have a distance of noid bone. Posterior and lateral is the apex par- 19.5±1.0 mm. Beside the anterior clivus is the tis petrosae of the temporal bone, and medial foramen lacerum, an irregular aperture formed is the basilar part of the occipital bone. The between the posterior clinoid process and the internal carotid arteries and the accompanying petrous apex with the opening tilting medioan- sympathetic nerves enter the cranium via the teriorly. The length of the foramen lacerum is upper part of the foramen (Figure 2).

3274 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation

Table 2. Measurement of the structures surrounding the hypoglossal canal Distance `X±s (mm) The length of the hypoglossal canal 7.7±0.8 The distance between the midpoint of the clival inferior rim to the line connecting the bilateral hypoglossal canals 4.5±1.6 The distance between the midpoint of the clival inferior rim to the left hypoglossal canal 16.7±2.1 The distance between the midpoint of the clival inferior rim to the right hypoglossal canal 17.6±1.0 Inner diameter of the hypoglossal canal 24.9±1.3 Outer diameter of the hypoglossal canal 32.1±1.9

Surgical simulation via the transnasal route to visualization of the dorsum sellae and the pos- the clivus terior clinoid process. These two structures define the superior boundary of the exposure. Transnasal surgery to the clivus is often per- The inferior border of the opened window is the formed through unilateral nose with a wider inferior rim of the clivus. The average distance nasal meatus. The opening of the sphenoidal between the superior and inferior borders is sinuses is located in between the superior 40.7±1.6 mm. nasal concha and the nasal septum, which serves as an ideal landmark for anatomical ref- Surgical simulation via the transoral route to erence. During the operation, the anterior spina the clivus ossis sphenoidalis may be preserved as the After the occipital joint of the atlas is exposed, landmark of the midline. Alternatively, the mid- the virtual drill is used to remove the clival bone line can be defined by the sellar floor or clival from the midline area of the inferior clivus. The recess. In the VR model, after opening the drilling begins from the inferior rim of the clivus sphenoidal sinuses, a virtual drill is used to and then moves upward toward the vertical line remove the anterior wall of the sphenoid sinus. formed by the bilateral hypoglossal canals. The While extending the drilling laterally in the ante- measurements which define the boundaries for rior wall, bone removal should be restricted the surgical window are shown in Table 2. within the medioinferior side of the pterygoid Careful drilling is necessary while removing the canal. It is also observed that the cavernous lateral bone. Caution should be taken to avoid part of the internal carotid artery causes a injuries to the hypoglossal nerve. bulge in the lateral wall of the sphenoid sinus. To visualize the structures adjacent to the cli- To expand the exposure upward, a part of the vus, drilling is done from the midline area of the hard palate and the posterior bone of the nasal clival bone so that the internal carotid arteries septum need to be removed. The inferior and are exposed in the midline region. The arteries anterior walls of the sphenoid sinus are drilled define the lateral boundaries for removal of the to expose the superior part of the clivus. Drilling clival bone. Drilling of the inferior wall of the should be done closely along the midline and sphenoid is then done so that the exposure gradually move laterally to prevent ruptures of extends to the middle and inferior parts of the the internal carotid arteries on the sides. In clival bone. To remain restricted within the lat- addition, the drilling needs to be horizontally eral boundaries, drilling in the bone area should restricted within the two internal carotid arter- proceed very slowly. In the VR system, each ies to avoid injuries to the inferior petrosal area is assigned a specific color. When the sur- sinus of the petrous oblique fissure. The resul- geon makes an error during drilling, an immedi- tant opened window exposes the entire clivus. ate change in the color(s) around the surgical When visualized from the oral region to the area will be recognized. For example, if the skull base, the brainstem and basilar arteries color red, which represents blood vessels, are readily observed in the cranium, as shown appears in the middle of the bone where drilling in Figure 4. is occurring, the surgeon will notice the color change to red immediately. Note that in some The simulation indicates that a safe area cases the clival bone is very thin (Figure 3). The opened for transoral surgery can be defined as measurements indicate that the average short- follows. The upper boundary is the sellar floor est distance between the bilateral boundaries and the lower boundary is the inferior rim of the is 18.0±1.8 mm. Right above the opened win- clivus. The average distance is 40.7±1.6 mm. dow is the pituitary gland, which prevents the When drilling the clival bone toward the lateral

3275 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation

3276 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation

Figure 4. Surgical stimulation via the transoral route to the clivus. A. At the inferior clivus, the virtual drill is used to remove the clival bone within the internal foramen of the hypoglossal canal; B. Removal of the clival bone between the bilateral hypoglossal canals exposes the anterior brainstem and the vertebral artery. Caution should be taken to avoid damage to the structures of the hypoglossal canal; C. Superior clivus exposed after removal of a bony part of the hard palate; D. The sphenoid exposed after the removal of the inferior and anterior walls; E. The pituitary gland and internal carotid arteries besides the clivus exposed after the removal of the sellar floor, the lateral wall of the sphenoid, and the posterior bone; F. The entire clival bone exposed in the opened window. The brainstem and basilar arteries behind the clivus were also observed. sides at the level between the sellar floor and vidual basis. The average lateral spacing is 9 the hypoglossal canals, the working area mm from the midline when drilling in the supe- should be restricted within the two internal rior and middle clivus. But the width can be nar- carotid arteries. The average distance is rower in some individuals according to the mea- 18.0±1.8 mm. When drilling toward the lateral surements from the VR model of the distances sides at the level between the hypoglossal between the bilateral boundaries for the poste- canals and the inferior clivus, the area should rior vertical part of the internal carotid arteries be limited within the internal foramen of hypo- and the vertical part at the sellar floor. Caution glossal canal. The average width of the window needs to be taken to identify the critical ana- at the level is 24.9±1.3 mm. tomical landmarks and only drill the bone of the clivus. The average distance between the inter- Discussion nal foramen of the hypoglossal canals is 24 mm. When drilling at the inferior clivus, the The clival VR model: the technique and the exposure should be kept strictly within the bor- features ders so as to keep the hypoglossal nerves The clivus is surrounded in very close proximity intact. by vital structures which make the anatomy in The reconstruction methods the clival area complicated. High quality images are required to establish the clival VR model in Surface rendering and volume rendering are order to achieve visualization and surgical sim- two commonly used methods for reconstruc- ulation. In this study we describe a VR model tion of anatomical structures from medical that we created to represent the anatomical imaging [16-18]. Surface rendering is a fast environment of the clival area and allow surgi- approach for reconstructing the intracranial cal simulation. Dual imaging modalities (i.e., blood vessels identified by CTA. It is efficient in CTA and MRI) helped identify the various struc- reconstruction, and has minimal hardware and tures with different contrasts and signal inten- software requirements. However, it results in sities so that the revealed anatomy is more edges that are not as clean as those obtained complete. CT was able to demonstrate the with volume rendering. In addition, it does not bone in great detail, and some parts of the contain information from the underlying tis- bone were color coded. The blood vessels visu- sues, and thus it is not feasible for clinical diag- alized with CTA had round lumens and less vari- nosis, preoperative evaluation, and surgery ability in diameter. MRI T1WI showed the brain- simulation. VR is based upon the method of stem and pituitary gland with the boundary volume rendering, which allows the accurate clearly defined. The VR model has considerable representation of the anatomical structures, advantages compared to conventional dissec- detailed visualization of the three spatial tion of corpses and 2-D cross-sectional imag- dimensions, and identification of the spatial es, because its use is unlimited and it provides relationships of an anatomical area in relation more information on three-dimensional spac- to common landmarks. However, the computa- es. And even more importantly, the model can tional loading of volume rendering is very be customized for individual patients and tai- exhaustive and requires much higher hardware lored according to the pathological condition standards. for preoperative surgery. Comparison of the transnasal and transoral In the surgical procedures, the window space routes opened for the clival operation is very critical. The window should be kept within the lateral Surgical operation in the clivus takes the ante- boundaries defined by the bilateral carotid rior course regardless of the transnasal or tran- arteries and the hypoglossal canals on an indi- soral route being taken. Understanding the

3277 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation anatomy and experiences with surgery is nec- Additionally, the model is unable to reveal the essary. To avoid damage to the surrounding dura, soft tissues and some cranial nerves, structures, it is critical to determine the mid- which affects the representation value and line. The VR model indicates that the bony thus its applicability for surgical guidance. Also, nasal septum and the vomer are located in the the three-dimensional measurements might be midline. These structures can be used as a ref- slightly different from those in real surgery, erence point. In the sphenoid sinus, the midline which is another shortcoming. Finally, in the can be determined by the sellar floor and the present study, the model was established from clival recess. If the protuberance of the internal the unaffected clivus of patients. Patients with carotid artery can be localized during the sur- a pathological clivus may be needed for refining gery, the gap between the bilateral protuber- the VR model. ances also helps to define the midline. The surgical space of the transoral route is relatively Conclusions larger than the transnasal space. The pharyn- geal tubercle is also found along the midline The complicated anatomy of the clival region when the inferior clivus is exposed during the makes clival surgery arduous. Traditional surgi- surgery. Access via the transoral route is rela- cal planning and research is often based upon tively efficient with better viewing of the entire the dissection of corpses and 2-D cross-sec- clivus. tional images. Three-dimensional information may be conceptualized in experienced sur- The value of the clival VR model in surgical geons, but is inaccessible to novices. The 3-D guidance clival model enables preoperative planning and stereography, which are very useful for inexpe- The simulation of the VR model offers a straight- rienced surgeons. In contrast to the intra-oper- forward, three-dimensional, and interactive ative neuronavigational system for guiding the understanding of the size and shape of the cli- surgeon during the surgery, our VR model is for vus, and its relationships with the surrounding preparing the surgeon at the preoperative blood vessels and bones. It also demonstrates stage. The measurements derived from our VR simulated operational procedures such as model are comparable to those of previous opening the surgical window, measuring the observations, which directly support the validi- exposure distance and angles, and determining ty of our method. The measurements can be the critical boundaries in relation to key struc- taken flexibly within the 3-D space beginning tures such as the brainstem and arteries. The and ending at any point. The flexible viewing information is very useful for planning minimal- and exploration will help the surgeon to gain a ly invasive neurosurgery [3, 19-21]. The VR VR impression and may bring about the déjà vu model helps to identify suitable landmarks and phenomenon when the surgeon performs the spacing with respect to the clival pathology so real surgery. The model is more objective and as to minimize the affected areas and maxi- thus is more likely to be accepted as standard. mize the resection of the lesion. It is envisioned The VR model may be considered as an aid to that digitalized VR modeling will be helpful for conventional surgical routines [26]. understanding the anatomy of the clivus and its surgical approaches by offering immediate Disclosure of conflict of interest results and unlimited practice at the preoperative stage. VR significantly saves cost and time None. in training neurosurgeons, and thus is increas- ingly being recognized as a future mainstream Address correspondence to: Dr. Shou-Sen Wang, procedure for preoperative planning and prac- Department of Neurosurgery, Fuzhou General Hos- tice [22-25]. pital, Fujian Medical University, Fuzhou 350025, China. Tel: +86 13950482966; Fax: +86-591-876- Limitations 40785; E-mail: [email protected]

There are inevitable differences between the References clival VR model and reality in clinical surgery. The removed and relocated tissues during sur- [1] Robison RA, Liu CY, Apuzzo ML. Man, mind, gery cannot be demonstrated in the model. The and machine: the past and future of virtual re- lack of tactile sense and proprioception is also ality simulation in neurologic surgery. World a disadvantage of VR simulation surgery. Neurosurg 2011; 76: 419-430.

3278 Int J Clin Exp Med 2014;7(10):3270-3279 Clival virtual reality surgical simulation

[2] Rosahl SK, Gharabaghi A, Hubbe U, Shahidi R, [15] Kockro RA, Serra L, Tseng-Tsai Y, Chan C, Yih- Samii M. Virtual reality augmentation in skull Yian S, Gim-Guan C, Lee E, Hoe LY, Hern N, No- base surgery. Skull Base 2006; 16: 59-66. winski WL. Planning and simulation of neuro- [3] Stadie AT, Kockro RA, Reisch R, Tropine A, Boor surgery in a virtual reality environment. Neu- S, Stoeter P, Perneczky A. Virtual reality system rosurgery 2000; 46: 118-135; discussion for planning minimally invasive neurosurgery. 135-137. Technical note. J Neurosurg 2008; 108: 382- [16] Low D, Lee CK, Dip LL, Ng WH, Ang BT, Ng I. 394. Augmented reality neurosurgical planning and [4] van Dongen KW, Ahlberg G, Bonavina L, Carter navigation for surgical excision of parasagittal, FJ, Grantcharov TP, Hyltander A, Schijven MP, falcine and convexity meningiomas. Br J Neu- Stefani A, van der Zee DC, Broeders IA. Euro- rosurg 2010; 24: 69-74. pean consensus on a competency-based vir- [17] Malone HR, Syed ON, Downes MS, D’Ambrosio tual reality training program for basic endo- AL, Quest DO, Kaiser MG. Simulation in neuro- scopic surgical psychomotor skills. Surg En- surgery: a review of computer-based simula- dosc 2011; 25: 166-171. tion environments and their surgical applica- [5] Wang SS, Xue L, Jing JJ, Wang RM. Virtual re- tions. Neurosurgery 2010; 67: 1105-1116. ality surgical anatomy of the sphenoid sin- [18] Sugimoto M, Yasuda H, Koda K, Suzuki M, Ya- us and adjacent structures by the transna- mazaki M, Tezuka T, Kosugi C, Higuchi R, Wa- sal approach. J Craniomaxillofac Surg 2012; tayo Y, Yagawa Y, Uemura S, Tsuchiya H, Azuma 40: 494-499. T. Image overlay navigation by markerless sur- [6] Goravalingappa R, Han JC, Mangiardi J, Lev- face registration in gastrointestinal, hepatobi- enson M. Endoscopic/Microscopic approach liary and pancreatic surgery. J Hepatobiliary to sphenopetroclival complex: an anatomical Pancreat Sci 2010; 17: 629-636. study. Skull Base Surg 1999; 9: 33-39. [19] Ferroli P, Tringali G, Acerbi F, Aquino D, Franzini [7] Caversaccio M, Langlotz F, Nolte LP, Häusler R. A, Broggi G. Brain surgery in a stereoscopic vir- Impact of a self-developed planning and self- tual reality environment: a single instituti- constructed navigation system on skull base on’s experience with 100 cases. Neurosurgery surgery: 10 years experience. Acta Otolaryngol 2010; 67: ons79-84. 2007; 127: 403-407. [20] Schulze F, Bühler K, Neubauer A, Kanitsar A, [8] Fatemi N, Dusick JR, Gorgulho AA, Mattozo CA, Holton L, Wolfsberger S. Intra-operative virtual Moftakhar P, De Salles AA, Kelly DF. Endonasal endoscopy for image guided endonasal trans- microscopic removal of clival chordomas. Surg sphenoidal pituitary surgery. Int J Comput As- Neurol 2008; 69: 331-338. sist Radiol Surg 2010; 5: 143-154. [9] Resch KD. Minimally invasive techniques in [21] Wong GK, Zhu CX, Ahuja AT, Poon WS. Cranio- neurosurgery: the transoral transpharyngeal tomy and clipping of intracranial aneurysm in a approach to the brain. Neurosurg Rev 1999; stereoscopic virtual reality environment. Neu- 22: 2-25; discussion 26-27. rosurgery 2007; 61: 564-68. [10] Stamm AC, Pignatari SS, Vellutini E. Transnasal [22] Agarwal N, Schmitt PJ, Sukul V, Prestigiacomo endoscopic surgical approaches to the clivus. CJ. Surgical approaches to complex vascular Otolaryngol Clin North Am 2006; 39: 639-656. lesions: the use of virtual reality and stereo- [11] Burkart CM, Theodosopoulos PV, Keller JT, Zi- scopic analysis as a tool for resident and stu- mmer LA. Endoscopic transnasal approach to dent education. BMJ Case Rep 2012; 2012. the clivus: a radiographic anatomical study. [23] Lemole GM Jr, Banerjee PP, Luciano C, Neck- Laryngoscope 2009; 119: 1672-1678. rysh S, Charbel FT. Virtual reality in neurosurgi- [12] Kimura F, Kim KS, Friedman H, Russell EJ, cal education: part-task ventriculostomy simu- Breit R. MR imaging of the normal and abnor- lation with dynamic visual and haptic feed- mal clivus. AJR Am J Roentgenol 1990; 155: back. Neurosurgery 2007; 61: 142-8. 1285-1291. [24] Lewis TM, Aggarwal R, Rajaretnam N, Gran- [13] Kockro RA, Reisch R, Serra L, Goh LC, Lee E, tcharov TP, Darzi A. Training in surgical onc- Stadie AT. Image-Guided Neurosurgery With ology - the role of VR simulation. Surg Oncol 3-Dimensional Multimodal Imaging Data on a 2011; 20: 134-139. Stereoscopic Monitor. Neurosurgery 2013; 72 [25] Zhao YC, Kennedy G, Yukawa K, Pyman B, Suppl 1: 78-88. O’Leary S. Can virtual reality simulator be used [14] Gu SX, Yang DL, Cui DM, Xu QW, Che XM, Wu as a training aid to improve cadaver temporal JS, Li WS. Anatomical studies on the temporal bone dissection? Results of a randomized bridging veins with Dextroscope and its appli- blinded control trial. Laryngoscope 2011; 121: cation in tumor surgery across the middle and 831-837. posterior fossa. Clin Neurol Neurosurg 2011; [26] Tan SS, Sarker SK. Simulation in surgery: a re- 113: 889-894. view. Scott Med J 2011; 56: 104-109.

3279 Int J Clin Exp Med 2014;7(10):3270-3279