Transoral robotic surgery of craniocervical junction and atlantoaxial ...

J Neurosurg Spine 12:13–18, 2010

Transoral robotic surgery of craniocervical junction and atlantoaxial spine: a cadaveric study Laboratory investigation *John Y. K. Lee, M.D.,1 Bert W. O’Malley Jr., M.D., 2 Jason G. Newman, M.D., 2 Gregory S. Weinstein, M.D., 2 Bradley Lega, M.D.,1 Jason Diaz, M.D., 2 and M. Sean Grady, M.D.1 Departments of 1Neurosurgery and 2Otolaryngology, University of Pennsylvania, Philadelphia, Pennsylvania Object. The goal of this study was to determine the potential role and current limitations of the da Vinci surgical robot in transoral decompression of craniocervical junction (CCJ). Methods. The da Vinci Surgical System was used in 2 cadaver heads with neck and clavicles intact. Both neurosurgeons and otolaryngologists familiar with the open microscopic procedure, as well as the transoral robotic surgical procedure, undertook dissection and decompression of the CCJ. Results. The robotic system provided superb illumination and 3D depth perception even several centimeters deep to the posterior oropharyngeal mucosa. The 30° endoscope improved cephalad visualization, eliminating the need to split the soft palate for exposure of the lower clivus. The “intuitive” nature of the da Vinci surgical robot arms provided an advantage in allowing the ability to suture the dura mater in a deep, dark corridor. Because visualization was excellent, tremor-free closure was possible. Conclusions. The authors’ findings suggest that transoral robotic surgery, with the da Vinci robot system, holds great potential for decompression of the CCJ as well as resection of both extra- and intradural tumors of this region. Further instrument development is necessary and continued investigation is warranted. (DOI: 10.3171/2009.7.SPINE08928)

Key Words • transoral surgery • robotic surgery • craniocervical junction • pannus

T

transoral approach is the most direct and effective means to decompress the CCJ. It is well suited to relieve compression from basilar invagination, congenital skull base malformations, extradural lesions such as rheumatoid pannus, or tumors such as chordomas and chondrosarcomas5 of the lower clivus/CCJ. This approach has been described and refined by Menezes and VanGilder,5 Menezes et al.,6 Crockard,1 and Hadley el. al.,3 but significant limitations and technical challenges remain. Specifically, if the transoral route is used for intradural pathological entities, such as a meningioma, or if an inadvertent durotomy occurs during extradural dissection, achieving a watertight closure of the dura mater in such a deep and narrow working channel is limited with current microscopic and endoscopic techniques. These considerations have led our group to explore an alternative approach. he

Abbreviations used in this paper: CCJ = craniocervical junction; TORS = transoral robotic surgery; VB = vertebral body. * Drs. Lee, O’Malley, Newman, and Weinstein contributed equally to the study and are thus considered first authors.

J Neurosurg: Spine / Volume 12 / January 2010

The use of robot-assisted surgery has gained significant support in multiple surgical specialties, including cardiac surgery, urology, obstetrics, gynecology, and, most recently, minimally invasive head and neck surgery. Proponents of robot-assisted surgery refer to the excellent 3D visualization and the “intuitive” surgical manual manipulation of the instruments. Our otolaryngology group has pioneered the world’s first TORS program. We have previously reported on the development of TORS in preclinical models.4,9–11,14 In addition, this transoral robotic approach has been successfully used to treat patients with laryngeal, glottic, tonsillar, and even infratemporal fossa lesions.12,15,16 Based on the success of transoral robotic surgery for these lesions, we explored the application of the da Vinci surgical robot (Intuitive Surgical Inc.) to decompress the CCJ in cadaveric models. The experiments discussed this paper were conductThis article contains some figures that are displayed in color online but in black and white in the print edition.

13

J. Y. K. Lee et al. ed to test the hypothesis that robotic surgical technology could be used to decompress the CCJ. We describe the details of the arrangement of the robotic implements, the structures we were able to dissect, and the specific requirements for new robotic equipment more germane to the problems of skull base surgery. Furthermore, cadaveric and animal studies are planned before we expand these techniques to human clinical trials.

Methods

The da Vinci Surgical System was used in 2 cadaver heads with neck and clavicles intact to most effectively mimic real operating room conditions. The heads were positioned supine without fixation. A Crowe-Davis retractor (Storz) was inserted into the oral cavity, resulting in no more than 4 cm of oral opening (Fig. 1). Two red rubber catheters were inserted through the nose, brought out laterally through the mouth, and clamped in position to maximize retraction of the soft palate. The surgical robot was positioned at the top of the table, cranial to the cadaveric head, to optimize the attack angle of the 3 robotic arms as they were directed anteroposteriorly/inferosuperiorly in the oral cavity (Fig. 2). The binocular endoscope arm was brought in on the midline with the 2 articulating arms entering laterally without compression of the buccal skin folds. An 8.5-mm 0° scope was used. A Maryland articulated dissector was placed in the left arm and a monopolar spatula-type electrocauterizer in the right. The operating surgeon docked at the da Vinci station and began with a midline incision in the posterior pharyngeal mucosa (Fig. 3). An assistant, observing the view of the surgeon on an adjacent monitor, provided suction with a standard Frazier tip instrument. The assistant stood to the right of the patient at the level of the thorax (Fig. 4). The assistant also monitored clearance of the robotic arms from the teeth. The anterior ring of C-1, the VB of C-2, and intervertebral spaces were identified. The eustachian tubes were identified and carefully avoided. Dissection proceeded quickly as the Maryland articulated dissector held tension on the mucosa and electrocautery was used to dissect through layers down to the C-1 ring and then inferiorly to the C-2 VB (Fig. 5). The oropharyngeal mucosa was cauterized using monopolar cautery, but a bipolar cautery is also available as either a Maryland or cardiac microbipolar forceps. Of note, we did not use mucosal retractors because of the physical barrier that this would have imposed on the freedom of movement of the EndoWrist arms, but had it become necessary, we could have placed retracting sutures in the mucosa to retract. The anterior longitudinal ligament was then divided with the EndoWrist Bovie electrocautery, exposing the anterior atlantooccipital membrane superiorly, the arch of C-1, and the dens and the VB of C-2. This dissection was controlled at the console by the operating surgeon with only minimal assistance from the bedside surgeon. Once the soft-tissue dissection was complete and the anatomy had been identified, the next stage of the procedure shifted from the primary surgeon at the da Vinci console to the assistant standing at the side of the cadaver. Currently there is no drill attachment for the robotic da 14

Fig. 1. The camera and arms are all inserted through the mouth, which is held open by transoral Crowe-Davis retractor. Red rubber catheters are used to retract the soft palate. The maximum diameter of interincisal opening was restricted to 4 cm.

Vinci arm, and hence, the bedside assistant completed the drilling using a standard Midas Rex electric drill with a matchstick bur (AM-8). The assistant was able to visualize the scene on the 2D flat-panel screen with superior illumination. The primary surgeon seated at the remote robotic console was able see in 3 dimensions and was able to assist and guide the removal of bone. The C-1 arch was removed with the drill by creating 2 troughs no more than 16 mm in maximum width (that is, medial border of the C-1 lateral mass).13 Once the C-1 arch was resected, the apical ligament was identified. A top-down drilling approach, as advocated by Haid,8 was used. Using a Kerrison punch and curette, the assistant accomplished final removal of the residual bone of the dens and the apical and alar ligaments (Fig. 6). The operating surgeon, who benefited from the 3D view available with the binocular endoscope, provided the corrections in the placement and direction of the dissection. The odontoidectomy was completed in this manner, exposing the underlying dura, thus completing the standard extradural decompression of rheumatoid pannus. The unique advantages of the da Vinci robot allowed

Fig. 2. The robotic arms are introduced transorally, angled cephalad toward the nasopharynx and cranial base.


Transoral robotic surgery of craniocervical junction

Fig. 3. Zero degree endoscopic view of the uvula and soft palate being retracted superiorly. The robotic arms are ready to dissect the posterior pharyngeal mucosa overlying C-1 and C-2.

us to carry forward and open the dura in a precise manner. Because the bone work was complete, the primary surgeon once again became the surgeon seated at the remote robotic console. Exposure of the underlying cervicomedullary junction proceeded with the use of articulated 5-mm Endo Wrist inserted into the right arm of the da Vinci robot (Fig. 7). The dural leaves were reflected, exposing both vertebral arteries and the anterior spinal artery (Fig. 8). Using the 0° scope alone, we could not view the intracranial vertebral artery. Hence, we switched to the 30°, 8.5-mm binocular endoscope. With this endoscope, the basion and lower clivus were visible. Using the robotic arms, tremor-free closure was attempted. With 2 articulated Maryland dissectors, we were able to close the dura primarily with interrupted 4-0 Vicryl sutures and U-clip nitinol sutures (Medtronic) (Fig. 9). Although interrupted sutures were possible in the dura at this depth, the dura of the midline clivus was very thin and did not hold suture well, and thus interrupted sutures were used. Although the dura could be reapproximated, a watertight closure was not possible. Dural patches were not attempted. In addition, mucosal closure was performed also with the da Vinci robotic arms. The mucosa was closed in a single layer using interrupted Vicryl sutures. All suture ties and U-clip ties were performed from the operating surgeon console utilizing the articulated hands of the robot.

Results

The difficulty of the transoral approach for odontoidectomy and access to the CVJ lies in the depth of critical structures and corresponding difficulty in obtaining adequate visualization to safely carry out dissection, as well as the narrowness of the working channel that limits the freedom with which a surgeon can manipulate instruments. The da Vinci robot overcomes the problem of visualization through superb illumination and 3D depth perception even several centimeters deep to the posterior oropharyngeal mucosa. This was achieved without J Neurosurg: Spine / Volume 12 / January 2010

Fig. 4. Schematic of the room setup, demonstrating the position of the operating surgeon at the robotic console and the assistant at the bedside.

elaborate measures taken to improve visualization such as splitting the mandible or incising the soft palate. The ergonomics of surgery with the da Vinci system are different from conventional microscopic or endoscopic techniques. The primary surgeon is seated at the robotic console and enjoys a 3D view while seated in a chair with complete control of the robot within an ergonomically designed console. The primary surgeon is thus perhaps most at ease with the working environment. In contrast, the assistant at the bedside has a more difficult time because the assistant has to look at the field and position his/her instruments around the robotic arms. In addition, the assistant has to alternate between looking at the operative field and looking up at the screen to assist effectively. Thus, da Vinci robotic surgery provides an ergonomic advantage for the primary surgeon and a disadvantage for the assistant surgeon compared with traditional open or microscopic approaches. During the approach, the eustachian tube, a source of morbidity if violated, was clearly identified and kept away from the mucosal flap. The lateral mass of C-1 and the occipitocervical joint capsule were clearly identified, and the excellent visualization allowed layers of tough ligament to be taken down carefully in sequence. Identification of the C-1 ring and C-2 VB, as well as the basion at the foramen magnum, was enhanced by the 3D depth perception provided by the binocular endoscope. The 0° endoscope provided excellent visualization of the atlas and axis without excessive retraction. The lower clivus was visualized as well, but only with the use of the 30° 15

J. Y. K. Lee et al.

Fig. 5. Exposure of the clivus, C-1, and base of C-2 after having dissected the soft tissue and anterior longitudinal ligament with the robotic arms.

angled endoscope; however, we could achieve better visualization of the mid- to lower clivus. Suture closure of the dura is difficult because of the deep location of the dura relative to the lateral masses of the C-1 atlas and the C-2 dens. The average width between the lateral masses of C-1, elegantly described by Tun et al.,13 has been measured at 16.1 ± 1.5 mm. To access the lateral aspect of the dens, the minimum bony drilling diameter is ~ 10.8 ± 1.1 mm. However, we recommend drilling as wide as the medial border of the lateral mass to maximize exposure if there is any plan to perform dural suturing. In addition, the depth of the C-1 ring is an average of 7.0 ± 1.2 mm. In addition, however, the C-2 dens process that must be removed to access the dura is on average 11.2 ± 1.0 mm (Fig. 10).2 Thus, the robotic hands must be able to manipulate in a channel that is ~ 16 mm wide and at least 18.2 mm deep (not including the ligaments). The height of the channel is variable depending on the distance from the basion to the lowest point of drilling into the C-2 VB during removal of

Fig. 6. Removal of the odontoid after drilling. Forceps inserted by the bedside assistant are being used to remove the free odontoid peg.

16

Fig. 7. Upper: Dural opening, demonstrating use of endoscissors. Lower: The articulated wrist of the Maryland dissector allows the scissors to be directed inferiorly without significantly changing the angle of the arm insertion.

the dens. These anatomical constraints limit one’s ability to suture effectively, although we were able to overcome this to some degree by changing the angle of suture to more craniocaudal as opposed to purely side to side. A 45° suture throw is technically easier in this location. Additionally, dural closure can be difficult because the clival dura is thin and does not hold suture well. Nevertheless, the EndoWrist robotic arms can be used to suture an autograft, allograft, or artificial dural patch to achieve a watertight closure. Fortunately, the “intuitive” nature of the da Vinci surgical arm provided an advantage: it allowed us to suture the dura in a deep, dark corridor because the visualization was excellent, and tremor-free closure was possible. Although this was a cadaver, we did time the second cadaveric procedure to get an estimate of complexity. The initial positioning of the mouth retractor, palatal retractor, and neck roll required 4 minutes. It then took 5.5 minutes to position the da Vinci S Surgical System Robot with the 8.5-mm endoscopic camera, the 5-mm EndoWrist Maryland bipolar forceps, and the 5-mm EndoWrist spatula in the mouth. Based on the videos, we timed the rest of the J Neurosurg: Spine / Volume 12 / January 2010

Transoral robotic surgery of craniocervical junction

Fig. 8. Intradural dissection with the robotic arms. The vertebral artery dominates the opening.

Fig. 9. Primary suture closure of the dura using 4-0 Vicryl suture.

procedure. The mucosal dissection with the robotic arms took ~ 10 minutes, and drilling by the assistant of the C-1 ring and C-2 dens took ~ 45 minutes. Opening and resuturing the dura took ~ 30 minutes, and the oropharyngeal mucosal closure required ~ 10 minutes. Hence, the entire procedure could be performed in < 2 hours.

to be developed and approved by the FDA. Nevertheless, the unique advantages of TORS include the articulated, grasping dissectors combined with excellent control and superb 3D visualization and illumination. Thus, robotic surgery can minimize one of the major morbidities of the transoral approach, specifically the risk of CSF leakage, because the robotic arms can be used to perform a tight dural closure with interrupted sutures. In some instances, anatomical variation among individuals may not permit the use of the transoral approach for patients in whom the dens and C-1 ring sit superior to the oral cavity in the nasopharynx; a transnasal approach or combined transnasal/transoral approach may be more appropriate in such cases.7,17,18 However, with the use of the 30° angled scope, the da Vinci robot may allow some additional flexibility in approaching these lesions because we were able to drill through the lower clivus as well in later anatomical studies (unpublished data). Hence, the transoral view with angled cameras that provide 3D, highmagnification view provides great potential for even those patients with greater degrees of basilar invagination.

Discussion

The transoral robotic surgical approach to the CCJ is technically feasible. The 0° and 30° angled, high-magnification, 3D optics permit generous visualization, even for the assistant who is looking at the 2D screen. The cadaveric dissections performed in this study allowed for both anatomical learning as well as the accrual of valuable surgical technique. At this time, a robot-assisted, transoral odontoidectomy is technically possible, although a fully robotic surgery will require the development of new tools for the da Vinci robotic arms. Specifically, high-speed drills, Kerrison punches, and curettes for osseous dissection are currently available only in prototype form and will need

Fig. 10. Computed tomography images of the odontoid and lateral masses of C-1. Distance A is measured at 16 mm, Distance B is the anterior ring of C-1, measured at 7 mm, and Distance C is the anteroposterior depth of the dens, measured at 12 mm on average. These values define the working space in 2 of 3 dimensions.


17

J. Y. K. Lee et al. Conclusions

In conclusion, our findings suggest that TORS holds great potential for decompression of the CCJ as well as resection of both extra- and intradural tumors of this region. Further instrument development is necessary and continued investigation is warranted. Disclaimer The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. References 1. Crockard HA: The transoral approach to the base of the brain and upper cervical cord. Ann R Coll Surg Engl 67:321–325, 1985 2. Doherty BJ, Heggeness MH: Quantitative anatomy of the second cervical vertebra. Spine 20:513–517, 1995 3. Hadley MN, Spetzler RF, Sonntag VK: The transoral approach to the superior cervical spine. A review of 53 cases of extradural cervicomedullary compression. J Neurosurg 71: 16–23, 1989 4. Hockstein NG, O’Malley BW Jr, Weinstein GS: Assessment of intraoperative safety in transoral robotic surgery. Laryngoscope 116:165–168, 2006 5. Menezes AH, VanGilder JC: Transoral-transpharyngeal approach to the anterior craniocervical junction. Ten-year experience with 72 patients. J Neurosurg 69:895–903, 1988 6. Menezes AH, VanGilder JC, Graf CJ, McDonnell DE: Craniocervical abnormalities. A comprehensive surgical approach. J Neurosurg 53:444–455, 1980 7. Messina A, Bruno MC, Decq P, Coste A, Cavallo LM, de Divittis E, et al: Pure endoscopic endonasal odontoidectomy: anatomical study. Neurosurg Rev 30:189–194, 2007 8. Mummaneni PV, Haid RW: Transoral odontoidectomy. Neurosurgery 56:1045–1050, 2005

18

9. O’Malley BW Jr, Weinstein GS: Robotic anterior and midline skull base surgery: preclinical investigations. Int J Radiat Oncol Biol Phys 69:S125–S128, 2007 10. O’Malley BW Jr, Weinstein GS: Robotic skull base surgery: preclinical investigations to human clinical application. Arch Otolaryngol Head Neck Surg 133:1215–1219, 2007 11. O’Malley BW Jr, Weinstein GS, Hockstein NG: Transoral robotic surgery (TORS): glottic microsurgery in a canine model. J Voice 20:263–268, 2006 12. O’Malley BW Jr, Weinstein GS, Snyder W, Hockstein NG: Transoral robotic surgery (TORS) for base of tongue neoplasms. Laryngoscope 116:1465–1472, 2006 13. Tun K, Kaptanoglu E, Cemil B, Karahan ST, Esmer AF, Elhan A: A neurosurgical view of anatomical evaluation of anterior C1-C2 for safer transoral odontoidectomy. Eur Spine J 17: 853–856, 2008 14. Weinstein GS, O’Malley BW Jr, Hockstein NG: Transoral robotic surgery: supraglottic laryngectomy in a canine model. Laryngoscope 115:1315–1319, 2005 15. Weinstein GS, O’Malley BW Jr, Snyder W, Hockstein NG: Transoral robotic surgery: supraglottic partial laryngectomy. Ann Otol Rhinol Laryngol 116:19–23, 2007 16. Weinstein GS, O’Malley BW Jr, Snyder W, Sherman E, Quon H: Transoral robotic surgery: radical tonsillectomy. Arch Otolaryngol Head Neck Surg 133:1220–1226, 2007 17. Welch WC, Kassam A: Endoscopically assisted transoraltranspharyngeal approach to the craniovertebral junction. Neurosurgery 52:1511–1512, 2003 18. Wu JC, Huang WC, Cheng H, Liang ML, Ho CY, Wong TT, et al: Endoscopic transnasal transclival odontoidectomy: a new approach to decompression: technical case report. Neurosurgery 63 (1 Suppl):ONSE92–ONSE94, 2008

Manuscript submitted December 22, 2008. Accepted July 29, 2009. Address correspondence to: John Y. K. Lee, M.D., Department of Neurosurgery, 3 Silverstein, 3400 Spruce Street, Philadelphia, Pennsylvania 19104. email: [email protected].
