Peer-Review Reports

The Supraorbital Endoscopic Approach for Aneurysms Robert Reisch1, Gerrit Fischer2,3, Axel Stadie4, Ralf Kockro1, Evaldas Cesnulis1, Nikolai Hopf 5

Key words - OBJECTIVE: To review our surgical experience in minimally invasive trans- - Intracranial aneurysms cranial endoscope-assisted microsurgical treatment of intracranial aneurysms, - Keyhole neurosurgery using the supraorbital keyhole craniotomy. - Minimally invasive neurosurgery - Supraorbital craniotomy - METHODS: The supraorbital keyhole approach was performed through an - Transcranial endoscope-assisted microneurosurgery eyebrow skin incision in 793 cases for treatment of 989 intracranial aneurysms. Of patients, 474 were operated on after subarachnoid hemorrhage, and 319 were Abbreviations and Acronyms operated on under elective conditions. After lateral frontobasal burr hole ISAT: International Subarachnoid Aneurysm Trial MCA: Middle cerebral artery trephination, a limited subfrontal craniotomy was created. To achieve adequate mRS: Modified Rankin scale intraoperative exposure through the limited approach, endoscopes were used TEAM: Transcranial endoscope-assisted routinely. Surgical outcome was assessed using the modified Rankin scale. microneurosurgery - RESULTS: The transcranial endoscope-assisted microneurosurgery technique 1 From the Centre for Endoscopic and was used routinely via a supraorbital approach. In 152 operations (19.1%), the Minimally Invasive Neurosurgery, Zurich, Switzerland; 2Department of Neurosurgery, Johannes endoscope provided important visual information in the vicinity of the aneurysm, Gutenberg-University Mainz, Mainz, Germany; 3Department revealing subsequent clip repositioning. The results of incidental aneurysms of Neurosurgery, University of Saarland, Homburg, Germany; were excellent with a modified Rankin scale score £2 in 96.52%. The overall 4Department of Neurosurgery, University Hospital Mannheim, Mannheim, Germany; and 5Department of outcome of ruptured aneurysms was good with a modified Rankin scale score £2 Neurosurgery, Katharinenhospital, Stuttgart, Germany in 72.2% of patients. There were no approach-related intraoperative or post- To whom correspondence should be addressed: operative complications. Robert Reisch, M.D., Ph.D. [E-mail: [email protected]] - CONCLUSIONS: The minimally invasive supraorbital keyhole approach Citation: World Neurosurg. (2014) 82, 6S:S130-S137. allowed safe surgical treatment of intracranial aneurysms, including after http://dx.doi.org/10.1016/j.wneu.2014.07.038 subarachnoid hemorrhage. The markedly improved endoscopic visualization Journal homepage: www.WORLDNEUROSURGERY.org increased the assessment of clip placement with ideal control of surrounding Available online: www.sciencedirect.com vessels including perforators for identification of incorrect clip position. 1878-8750/$ - see front matter ª 2014 Published by Elsevier Inc.

INTRODUCTION the subarachnoid spaces may decrease the Several cases of insufficient aneurysm oc- The initial data from the International risk of cerebral vasospasm and chronic clusion and postinterventional aneurysm Subarachnoid Aneurysm Trial (ISAT) hydrocephalus (14, 17, 20-22, 24, 29, 43, recanalization were reported associated published in 2002 showed a significant 46, 47, 53). With an additional opening of with increased risk of rebleeding (8, 33, superiority of endovascular coiling the lamina terminalis, the intracranial ce- 44, 49). compared with surgical clipping as rebrospinal fluid circulation also can be Nevertheless, operative therapy requires defined by the proportion of patients dead effectively improved (3, 27, 45). An oper- a surgical approach involving manipula- or disabled at 1 year in a carefully selected ative approach allows adequate optical tion and retraction of the cortical surface group of patients deemed suitable for exposure of the individual anatomy of the and functionally relevant neurovascular either therapy (31). The results of this aneurysm, with safe assessment of perfo- structures. Almost all neurosurgical cen- randomized, prospective, international rators and neighboring neurovascular ters included in ISAT used standard controlled trial represented a landmark structures (29, 33). In the case of rerupture microneurosurgical approaches to treat and radical change in the treatment of the aneurysm, immediate control of the ruptured aneurysm (31). We hypothe- of intracranial aneurysms (6, 9, 10, 28, 32, bleeding is possible (19). In addition, size that the reason for the significant 33, 48). surgical clipping of the aneurysm offers a superiority of endovascular coiling This significant superiority of interven- high reconstructive capacity of the vessel compared with surgical therapy in ISAT tional therapy is difficult to comprehend and high reliability of the occlusion was the surgical morbidity and mortality from a surgical point of view, particularly resulting in minimal risk of postoperative of “standard,” large surgical approaches after comparison of both methods. Using rebleeding (39). Interventional therapy that were usually employed in this study surgical exposure, operative removal of cannot offer careful exploration of the (12). We believe that operative clipping as blood clots with rinsing and cleaning of subarachnoid spaces or the aneurysm. treatment of intracranial aneurysms can be

S130 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.038 PEER-REVIEW REPORTS ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS improved if surgeons are able to reduce its (e.g., clip appliers, scissors, suction de- approach-related complications allowing vices) can effectively resolve this short- minimally invasive and maximally effective coming (13, 35-37, 39, 42). aneurysm closure. The most effective so- The most important disadvantage of lution for reducing intraoperative manip- small, less invasive keyhole approaches is ulation and retraction is the use of the loss of intraoperative light and sight minimally invasive keyhole approaches in causing significantly reduced optical con- neurosurgery (7, 11, 23, 30, 35-38, 41, 49). trol during surgery (39). For the purpose of However, marked reduction of the crani- bringing light into the surgical field, the otomy size may result in different short- optical properties of surgical microscopes comings during the procedure (39). can be effectively supplemented by the Because of the predefined direction of intraoperative use of endoscopes (5, 7, the operative exposure, the surgical 11-13, 15, 19, 23, 30, 37-39, 49). The main corridor cannot be changed intra- advantages of endoscopes are the operatively. Preoperative planning of the increased light intensity, broadening of approach, including 1) thorough evalua- the viewing angles, enlarged focus range, Figure 2. Transcranial endoscope-assisted microneurosurgery—TEAM-work between tion of preoperative diagnostic imaging of and clear depiction of pathoanatomic de- microscope and endoscope. the lesion with respect to the individual tails in close-up positions (Figure 2). anatomy of the patient, 2) definition of the size and site of the tailored craniotomy, After interdisciplinary discussion with 3) positioning of the patient according to MATERIALS AND METHODS the interventional neuroradiologist, surgi- the planned surgical corridor, and 4) skin- We retrospectively evaluated 793 consecu- cal treatment was chosen when endovas- to-skin performance of the exact tive cases of intracranial aneurysms oper- cular coiling was deemed technically not approach, is of particular importance in ated through a supraorbital keyhole feasible. In every case, the surgical keyhole surgery of intracranial aneurysms craniotomy. There were 269 male patients approach was determined after careful (11, 12, 37, 46). An additional problem is and 524 female patients; patient age preoperative study of diagnostic images to the application and maneuverability of ranged from 14e82 years (mean age, 51.8 determine the least traumatic access to the conventional instruments; the use of such years). Of procedures, 474 were performed lesion taking into consideration the indi- instruments becomes limited if the size of following an acute subarachnoid hemor- vidual anatomy of the patient. To improve the craniotomy is <15 mm (Figure 1). The rhage, and 319 were performed on patients intraoperative visualization and optical application of special keyhole-adapted with aneurysms that were found control during surgical manipulation, we slender microsurgical instruments incidentally. routinely used the technique of trans- cranial endoscope-assisted micro- neurosurgery (TEAM). The endoscopic imaging was evaluated with respect to the different routes that are available for the endoscope (e.g., the space between the eloquent neurovascular structures). The endoscopes were used for 1) intraoperative anatomic orientation, 2) assessment of the individual anatomy of the aneurysm including small perforators, and 3) control of clip position including the evaluation of neck occlusion or reconstructive capacity of the clip.

Supraorbital Keyhole Technique After positioning the patient supine, anatomic landmarks of the frontal area, such as the supraorbital foramen, tempo- ral line, level of the frontal cranial base, impression of the sylvian fissure, and zygomatic arch, are determined. Based on Figure 1. (A) Photograph comparing a conventional (left) and slender-type clip applier (Aesculap AG, this careful anatomic surface orientation, Tuttlingen, Germany). (B) When used in keyhole conditions, the conventional instrument cannot be the borders of the craniotomy and place- maneuvered, and placement of the clip is not controllable. (C) The tube shaft applier can be used ment of the individual skin incision are within the narrow corridor; the jaws of the clip are well seen allowing safe aneurysm closure. defined.

WORLD NEUROSURGERY 82 [6S]: S130-S137, DECEMBER 2014 www.WORLDNEUROSURGERY.org S131 PEER-REVIEW REPORTS ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS

After facultative use of neuro- muscles are retracted with sutures and C-shaped form and retracted in a basal monitoring, neuronavigation, and intra- hooks. A single frontobasal burr hole is direction, with minimal exploration of the operative imaging, the skin incision is made using a high-speed drill, avoiding brain surface (Figure 3F). started laterally from the supraorbital penetration of the orbit (Figure 3C). After incisura within the eyebrow. To achieve an minimal enlargement of the hole with a optimal cosmetic result, the incision thin Kerrison punch, a straight line is cut RESULTS should follow the orbital rim. To avoid with a high-speed craniotome parallel to Using the supraorbital keyhole approach, frontal numbness, the skin incision the orbital rim in a lateral-to-medial di- 989 aneurysms in 793 patients were should not extend medially to the rection. The craniotomy is completed with treated. There were 38 giant aneurysms, supraorbital nerve. The subcutaneous a C-shaped incision. A limited craniotomy and 53 patients had space-occupying he- dissection is continued in the frontal approximately 2 cm 1.5 cm is created matomas. Incomplete clipping was ach- Â direction to achieve optimal exposure (Figure 3D). A critical stage of the crani- ieved in 19 cases (3.3%) with complex of the frontolateral region. The frontal otomy after removal of the bone flap is aneurysm anatomy, making additional muscle is cut with a monopolar knife high-speed drilling of the inner edge of interventional treatment necessary. The parallel to the orbital rim in a medial-to- the bone above the orbital rim under overall outcome of the acute cases on lateral direction (Figure 3A). As the tem- protection of the dura mater (Figure 3E). follow-up examination was good (modi- poral line is reached with the monopolar Careful removal of this inner bone edge fied Rankin scale [mRS] score 2) in  knife, the blade is turned 90 degrees. The can significantly increase the angle for 72.2% and poor (mRS score 3) in 27.8%.  incision follows the temporal line in a visualization and manipulation. Small There were 319 operations performed on basal direction to the zygomatic process of osseous extensions of the superficial incidentally found aneurysms or as the frontal bone. The temporalis muscle is orbital roof, termed juga cerebralia, scheduled elective procedures. The surgi- dissected laterally; muscular mobilization should also be drilled extradurally to cal results were good (mRS score 2) in  is restricted to a necessary minimum obtain optimal intradural visualization. 96.6% and poor (mRS score 3) in 3.4%  (Figure 3B), The frontal and temporal The dura mater is opened in a simple of the cases. The TEAM technique was

Figure 3. (A) After skin incision within the eyebrow, the frontal muscle is of the dura mater, a straight line is cut in a lateral-to-medial direction, and cut with a monopolar knife parallel to the orbital rim in a medial-to-lateral the craniotomy is then completed with a C-shaped incision. (E) An essential direction. (B) The temporalis muscle is dissected laterally; muscular step of the approach is drilling of the inner edge of the bone above the mobilization is restricted to a necessary minimum. (C) The frontal and orbital rim, increasing the angle for visualization and manipulation. (F) The temporal muscles are retracted with sutures and hooks, and a lateral dura mater is opened simply in a curved way and retracted in a basal frontobasal burr hole is made using a high-speed drill. (D) After mobilization direction, with minimal exploration of the brain surface.

S132 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.038 PEER-REVIEW REPORTS ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS used routinely. Endoscopes were used mainly to visualize the target area before and after clipping and rarely for actual endoscope-controlled clipping pro- cedures. In 152 operations (19.1%), endoscopy revealed suboptimal or incor- rect clip position with 1) residual neck, 2) narrowed vessel, or 3) occluded perforator, which was poorly seen or not seen at all with the microscope. In all cases, clip position was subsequently corrected; the markedly improved endoscopic visualiza- tion increased the likelihood of controlling ideal aneurysmal closure.

Illustrative Case A 33-year-old woman whose sister had experienced severe subarachnoid hemor- rhage underwent neurologic examination that included magnetic resonance imaging of the brain. Imaging detected bilateral aneurysms of the middle cerebral artery (MCA). There were no signs of subarach- noid hemorrhage. Because of an irregular aneurysm sur- face, the family history, and the patient’s anxiety, the decision was made to treat the aneurysms. After performing digital sub- traction angiography and an interdisci- plinary discussion with the interventional neuroradiologists concerning the treat- Figure 4. (A) Preoperative angiography showing nonruptured bilateral aneurysms. The left-sided ment modality, surgical treatment was middle cerebral artery aneurysm originates near the early temporal branch, and the right-sided chosen. Factors favoring surgery were the aneurysm originates at the middle cerebral artery bifurcation. (B) After surgery, digital subtraction small size of the left-sided aneurysm, the angiography reveals no residual aneurysm. unfavorable aspect ratio of the dome and neck of the right-sided aneurysm, and the Endoscopic inspection verified the aneu- microscopic control, immediately closing patient’s request for surgical therapy rysm neck and its relationship to the early the aneurysm. The use of a tube-shaft clip (Figure 4A). Evaluation of magnetic reso- temporal branch (Figure 6B). A straight applier in the narrow corridor was crucial nance imaging and angiographic studies bayonet-shaped clip was placed under (Figure 6C). Complete aneurysm closure including three-dimensional planning software demonstrated that the left-sided aneurysm was proximally located near the early temporal branch. The right-sided aneurysm originated more distally at the MCA bifurcation (Figure 5). A right-sided supraorbital subfrontal exposure was chosen, treating both aneurysms through a single minimally invasive approach. After performing the supraorbital keyhole approach (Figure 3), the supra- sellar cisterns were opened, and the contralateral internal carotid artery was approached (Figure 6A). Gentle retraction was used; the elevator was placed between the frontal lobe and olfactory nerve, Figure 5. (A) Three-dimensional observation of bilateral aneurysms demonstrating the relationship of avoiding stretching the fila olfactoria. The the optic nerve and arterial vessels to the bony skull base structures allowing precise and fi comprehensive surgical planning. (B) Virtual inspection through the right-sided keyhole craniotomy contralateral sylvian ssure was opened, reveals that both aneurysms are safely approachable (Dextroscope; Volume Interactions, Singapore). approaching the left-sided aneurysm.

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was controlled with the help of the endo- scope (Figure 6D). The right sylvian fissure was opened without using the brain retractor. With microscopic visualization, the temporal branch of the MCA could not be visualized behind the dome of the aneurysm (Figure 6E); however, this hid- den part of the field was ideally managed with endoscopic assistance (Figure 6F). After successful clipping without the use of a retractor (Figure 6G), the clip position was endoscopically controlled, confirming reliable aneurysm closure without nar- rowing the MCA bifurcation surrounding the perforators (Figure 6H). Patency of the MCA branches was confirmed with Doppler sonography and indocyanine green angiography. Using the TEAM technique, both aneurysms could be completely closed through the one-sided limited keyhole approach. The patient had an uneventful recovery. Postoperative examination revealed no neurologic symptoms. computed tomog- raphy scan showed no intracranial com- plications and optimal repositioning of the bone flap. Cerebral angiography showed complete closure of both aneu- rysms (Figure 4B). The patient was able to return to her previous employment, and the cosmetic result was excellent.

DISCUSSION Since the beginning of neurosurgery, it has been widely accepted that exposure of brain tissue for several hours during sur- gery using extended craniotomies results in injury of the cortical surface by non- physiologic surroundings, including room air, irrigation, cover material, and spatula pressure (51). In addition, it has been shown in many experimental and clinical studies that brain retraction causes sig- nificant intraoperative trauma to brain tissue and may lead to permanent neuro- logic deficits (1, 2, 4, 25, 52). To minimize Figure 6. Intraoperative photographs showing critical steps of the procedure. (A) First, the opposite internal carotid artery was approached, and the sylvian fissure was exposed. (B) The anatomy of the brain retraction, various methods have left-sided aneurysm was investigated with the endoscope. After clipping with a tube-shaft been proposed (e.g., application of special instrument, secured by safe proximal control (C), endoscopic control revealed complete occlusion anesthetic techniques to achieve brain without narrowing of the parent vessels (D). (E) Next, the right middle cerebral artery was approached, but the temporal branch could not be seen behind the aneurysm dome and sphenoid relaxation, individual brain retractor sys- wing. With the endoscope, this hidden part could optimally be visualized (F), allowing safe clip tems, unusual positioning techniques of application (G). (H) The last endoscopic investigation showed complete closure without tightening the patient) (12, 13, 16, 18, 50). However, the middle cerebral artery bifurcation. ICA, internal carotid artery; CN II, optic nerve; ETB, early temporal branch; FB, frontal branch; TB, temporal branch. best retraction is no retraction. Careful choice of an adequate, least invasive

S134 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.038 PEER-REVIEW REPORTS ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS surgical approach with minimal brain along with other neuroendoscopic tech- endoscopes is mandatory for adequate exploration and dissection without the use niques, experienced an enormous revival in visualization, especially for control of clip of a retractor may result in a significant the 1990s (11-13, 15, 19, 37, 39, 42). At this placement and assessment of surrounding reduction of trauma to intracranial struc- time, Perneczky developed and refined the perforators. In 19.1% of our cases, tures (25, 37, 38). concept of endoscopic and endoscope- endoscopy revealed suboptimal clip posi- With the excellent diagnostic capabil- assisted neurosurgery using limited tion with residual neck, narrowed parent ities of digital subtraction angiography, keyhole approaches in transcranial neuro- vessel, or occluded peforator that was not three-dimensional angiography, surgery. As pioneer in minimal invasive clearly detected with the microscope. computed tomography, and MRI currently techniques, Perneczky became the teacher Endoscopic visualization increased mark- available, one can demonstrate and clarify of countless residents and international edly the likelihood of controlling optimal the individual spatial anatomy of a patient fellows in the Neurosurgical Department of aneurysmal closure and consequently including the smallest details. Anatomi- the University Mainz, Germany. achieving better surgical results. cally suitable corridors for surgical The TEAM technique enables neuro- dissection can be described and discussed surgeons to approach deep-seated regions ACKNOWLEDGMENTS in a meticulous preoperative planning through narrow anatomic windows, TEAM technique involves real teamwork. procedure. With the knowledge of the in- without excessive retraction of sensitive We express our gratitude to our colleagues dividual anatomic details of a specific pa- neurovascular structures. The endoscopic in the Clinic Hirslanden Zurich; in the tient, it is possible to perform a tailored pictures allow illumination and inspection University Hospitals Mainz, Homburg, and surgical procedure reducing the size of the of angles in hidden parts of the surgical Mannheim; and in the Katharinenhospital skin incision, the craniotomy, and the field and, owing to the enormous optical Stuttgart. Supraorbital craniotomy for extent of retraction and trauma to the depth of field of modern endoscopes, intracranial aneurysms was first used and brain surface to a minimum. In recent provide an almost three-dimensional described by our late teacher and mentor, years, the ability to plan specific ap- aspect of anatomic structures. Frequent Axel Perneczky. This article is dedicated to proaches has been improved further by training of spatial eye-hand coordination, him with deep grief and infinite respect. using three-dimensional graphic tools of which is necessary for all endoscope- radiologic image processing consoles or assisted microsurgical procedures, enables REFERENCES planning software of surgical navigation neurosurgeons to perform minimally systems. We have also worked extensively invasive, maximally effective procedures. 1. 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S136 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.038 PEER-REVIEW REPORTS ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS

51. Wilson DH: Limited exposure in cerebral neuro- monkeys resolves because of loss of and encase- Received 19 September 2013; accepted 25 July 2014 surgery. Technical note. J Neurosurg 34:102-106, ment of subarachnoid blood clot. Stroke 32: Citation: World Neurosurg. (2014) 82, 6S:S130-S137. 1971. 1868-1874, 2001. http://dx.doi.org/10.1016/j.wneu.2014.07.038 52. Yokoh A, Sugita K, Kobayashi S: Clinical study of Journal homepage: www.WORLDNEUROSURGERY.org brain retraction in different approaches and dis- Conflict of interest statement: The authors declare that the Available online: www.sciencedirect.com eases. Acta Neurochir 87:134-139, 1987. article content was composed in the absence of any 1878-8750/$ - see front matter ª 2014 Published by Elsevier commercial or financial relationships that could be construed 53. Zhang ZD, Yamini B, Komuro T, Ono S, Johns L, Inc. as a potential conflict of interest. Marton LS, Weir B, MacDonald RL: Vasospasm in

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