The Supraorbital Endoscopic Approach for Aneurysms

Robert Reisch1, Gerrit Fischer2,3, Axel Stadie4, Ralf Kockro1, Evaldas Cesnulis1, Nikolai Hopf 5

INTRODUCTIONThe initial data from the InternationalSubarachnoid Aneurysm Trial (ISAT)published in 2002 showed a significantsuperiority of endovascular coilingcompared with surgical clipping asdefined by the proportion of patients deador disabled at 1 year in a carefully selectedgroup of patients deemed suitable foreither therapy (31). The results of thisrandomized, prospective, internationalcontrolled trial represented a landmarkand radical change in the treatmentof intracranial aneurysms (6, 9, 10, 28, 32,33, 48).This significant superiority of interven-

tional therapy is difficult to comprehendfrom a surgical point of view, particularlyafter comparison of both methods. Usingsurgical exposure, operative removal ofblood clots with rinsing and cleaning of

the subarachnoid spaces may decrease therisk of cerebral vasospasm and chronichydrocephalus (14, 17, 20-22, 24, 29, 43,46, 47, 53). With an additional opening ofthe lamina terminalis, the intracranial ce-rebrospinal fluid circulation also can beeffectively improved (3, 27, 45). An oper-ative approach allows adequate opticalexposure of the individual anatomy of theaneurysm, with safe assessment of perfo-rators and neighboring neurovascularstructures (29, 33). In the case of reruptureof the aneurysm, immediate control ofbleeding is possible (19). In addition,surgical clipping of the aneurysm offers ahigh reconstructive capacity of the vesseland high reliability of the occlusionresulting in minimal risk of postoperativerebleeding (39). Interventional therapycannot offer careful exploration of thesubarachnoid spaces or the aneurysm.

Several cases of insufficient aneurysm oc-clusion and postinterventional aneurysmrecanalization were reported associatedwith increased risk of rebleeding (8, 33,44, 49).Nevertheless, operative therapy requires

a surgical approach involving manipula-tion and retraction of the cortical surfaceand functionally relevant neurovascularstructures. Almost all neurosurgical cen-ters included in ISAT used standardmicroneurosurgical approaches to treatthe ruptured aneurysm (31). We hypothe-size that the reason for the significantsuperiority of endovascular coilingcompared with surgical therapy in ISATwas the surgical morbidity and mortalityof “standard,” large surgical approachesthat were usually employed in this study(12). We believe that operative clipping astreatment of intracranial aneurysms can be

-OBJECTIVE: To review our surgical experience in minimally invasive trans-cranial endoscope-assisted microsurgical treatment of intracranial aneurysms,using the supraorbital keyhole craniotomy.

-METHODS: The supraorbital keyhole approach was performed through aneyebrow skin incision in 793 cases for treatment of 989 intracranial aneurysms.Of patients, 474 were operated on after subarachnoid hemorrhage, and 319 wereoperated on under elective conditions. After lateral frontobasal burr holetrephination, a limited subfrontal craniotomy was created. To achieve adequateintraoperative exposure through the limited approach, endoscopes were usedroutinely. Surgical outcome was assessed using the modified Rankin scale.

-RESULTS: The transcranial endoscope-assisted microneurosurgery techniquewas used routinely via a supraorbital approach. In 152 operations (19.1%), theendoscope provided important visual information in the vicinity of the aneurysm,revealing subsequent clip repositioning. The results of incidental aneurysmswere excellent with a modified Rankin scale score £2 in 96.52%. The overalloutcome of ruptured aneurysms was good with a modified Rankin scale score £2in 72.2% of patients. There were no approach-related intraoperative or post-operative complications.

-CONCLUSIONS: The minimally invasive supraorbital keyhole approachallowed safe surgical treatment of intracranial aneurysms, including aftersubarachnoid hemorrhage. The markedly improved endoscopic visualizationincreased the assessment of clip placement with ideal control of surroundingvessels including perforators for identification of incorrect clip position.

Key words- Intracranial aneurysms- Keyhole neurosurgery- Minimally invasive neurosurgery- Supraorbital craniotomy- Transcranial endoscope-assistedmicroneurosurgery

Abbreviations and AcronymsISAT: International Subarachnoid Aneurysm TrialMCA: Middle cerebral arterymRS: Modified Rankin scaleTEAM: Transcranial endoscope-assistedmicroneurosurgery

From the 1Centre for Endoscopic andMinimally Invasive Neurosurgery,

Zurich, Switzerland; 2Department of Neurosurgery, JohannesGutenberg-University Mainz, Mainz, Germany; 3Departmentof Neurosurgery, University of Saarland, Homburg, Germany;4Department of Neurosurgery, University HospitalMannheim, Mannheim, Germany; and 5Department ofNeurosurgery, Katharinenhospital, Stuttgart, Germany

To whom correspondence should be addressed:Robert Reisch, M.D., Ph.D.[E-mail: robert.reisch@hirslanden.ch]

Citation: World Neurosurg. (2014) 82, 6S:S130-S137.http://dx.doi.org/10.1016/j.wneu.2014.07.038

Journal homepage: www.WORLDNEUROSURGERY.org

Available online: www.sciencedirect.com

1878-8750/$ - see front matter ª 2014 Published by ElsevierInc.

S130 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.07.038

Peer-Review Reports

improved if surgeons are able to reduce itsapproach-related complications allowingminimally invasive and maximally effectiveaneurysm closure. The most effective so-lution for reducing intraoperative manip-ulation and retraction is the use ofminimally invasive keyhole approaches inneurosurgery (7, 11, 23, 30, 35-38, 41, 49).However, marked reduction of the crani-otomy size may result in different short-comings during the procedure (39).Because of the predefined direction of

the operative exposure, the surgicalcorridor cannot be changed intra-operatively. Preoperative planning of theapproach, including 1) thorough evalua-tion of preoperative diagnostic imaging ofthe lesion with respect to the individualanatomy of the patient, 2) definition of thesize and site of the tailored craniotomy,3) positioning of the patient according tothe planned surgical corridor, and 4) skin-to-skin performance of the exactapproach, is of particular importance inkeyhole surgery of intracranial aneurysms(11, 12, 37, 46). An additional problem isthe application and maneuverability ofconventional instruments; the use of suchinstruments becomes limited if the size ofthe craniotomy is <15 mm (Figure 1). Theapplication of special keyhole-adaptedslender microsurgical instruments

(e.g., clip appliers, scissors, suction de-vices) can effectively resolve this short-coming (13, 35-37, 39, 42).The most important disadvantage of

small, less invasive keyhole approaches isthe loss of intraoperative light and sightcausing significantly reduced optical con-trol during surgery (39). For the purpose ofbringing light into the surgical field, theoptical properties of surgical microscopescan be effectively supplemented by theintraoperative use of endoscopes (5, 7,11-13, 15, 19, 23, 30, 37-39, 49). The mainadvantages of endoscopes are theincreased light intensity, broadening ofthe viewing angles, enlarged focus range,and clear depiction of pathoanatomic de-tails in close-up positions (Figure 2).

MATERIALS AND METHODSWe retrospectively evaluated 793 consecu-tive cases of intracranial aneurysms oper-ated through a supraorbital keyholecraniotomy. There were 269 male patientsand 524 female patients; patient ageranged from 14e82 years (mean age, 51.8years). Of procedures, 474 were performedfollowing an acute subarachnoid hemor-rhage, and 319 were performed on patientswith aneurysms that were foundincidentally.

After interdisciplinary discussion withthe interventional neuroradiologist, surgi-cal treatment was chosen when endovas-cular coiling was deemed technically notfeasible. In every case, the surgicalapproach was determined after carefulpreoperative study of diagnostic images todetermine the least traumatic access to thelesion taking into consideration the indi-vidual anatomy of the patient. To improveintraoperative visualization and opticalcontrol during surgical manipulation, weroutinely used the technique of trans-cranial endoscope-assisted micro-neurosurgery (TEAM). The endoscopicimaging was evaluated with respect to thedifferent routes that are available for theendoscope (e.g., the space between theeloquent neurovascular structures). Theendoscopes were used for 1) intraoperativeanatomic orientation, 2) assessment of theindividual anatomy of the aneurysmincluding small perforators, and 3) controlof clip position including the evaluation ofneck occlusion or reconstructive capacityof the clip.

Supraorbital Keyhole TechniqueAfter 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, andzygomatic arch, are determined. Based onthis careful anatomic surface orientation,the borders of the craniotomy and place-ment of the individual skin incision aredefined.

Figure 1. (A) Photograph comparing a conventional (left) and slender-type clip applier (Aesculap AG,Tuttlingen, Germany). (B) When used in keyhole conditions, the conventional instrument cannot bemaneuvered, and placement of the clip is not controllable. (C) The tube shaft applier can be usedwithin the narrow corridor; the jaws of the clip are well seen allowing safe aneurysm closure.

Figure 2. Transcranial endoscope-assistedmicroneurosurgery—TEAM-work betweenmicroscope and endoscope.

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-monitoring, neuronavigation, and intra-operative imaging, the skin incision isstarted laterally from the supraorbitalincisura within the eyebrow. To achieve anoptimal cosmetic result, the incisionshould follow the orbital rim. To avoidfrontal numbness, the skin incisionshould not extend medially to thesupraorbital nerve. The subcutaneousdissection is continued in the frontaldirection to achieve optimal exposureof the frontolateral region. The frontalmuscle is cut with a monopolar knifeparallel to the orbital rim in a medial-to-lateral direction (Figure 3A). As the tem-poral line is reached with the monopolarknife, the blade is turned 90 degrees. Theincision follows the temporal line in abasal direction to the zygomatic process ofthe frontal bone. The temporalis muscle isdissected laterally; muscular mobilizationis restricted to a necessary minimum(Figure 3B), The frontal and temporal

muscles are retracted with sutures andhooks. A single frontobasal burr hole ismade using a high-speed drill, avoidingpenetration of the orbit (Figure 3C). Afterminimal enlargement of the hole with athin Kerrison punch, a straight line is cutwith a high-speed craniotome parallel tothe orbital rim in a lateral-to-medial di-rection. The craniotomy is completed witha C-shaped incision. A limited craniotomyapproximately 2 cm ! 1.5 cm is created(Figure 3D). A critical stage of the crani-otomy after removal of the bone flap ishigh-speed drilling of the inner edge ofthe bone above the orbital rim underprotection of the dura mater (Figure 3E).Careful removal of this inner bone edgecan significantly increase the angle forvisualization and manipulation. Smallosseous extensions of the superficialorbital roof, termed juga cerebralia,should also be drilled extradurally toobtain optimal intradural visualization.The dura mater is opened in a simple

C-shaped form and retracted in a basaldirection, with minimal exploration of thebrain surface (Figure 3F).

RESULTSUsing the supraorbital keyhole approach,989 aneurysms in 793 patients weretreated. There were 38 giant aneurysms,and 53 patients had space-occupying he-matomas. Incomplete clipping was ach-ieved in 19 cases (3.3%) with complexaneurysm anatomy, making additionalinterventional treatment necessary. Theoverall outcome of the acute cases onfollow-up examination was good (modi-fied Rankin scale [mRS] score "2) in72.2% and poor (mRS score #3) in 27.8%.There were 319 operations performed onincidentally found aneurysms or asscheduled elective procedures. The surgi-cal results were good (mRS score "2) in96.6% and poor (mRS score #3) in 3.4%of the cases. The TEAM technique was

Figure 3. (A) After skin incision within the eyebrow, the frontal muscle iscut with a monopolar knife parallel to the orbital rim in a medial-to-lateraldirection. (B) The temporalis muscle is dissected laterally; muscularmobilization is restricted to a necessary minimum. (C) The frontal andtemporal muscles are retracted with sutures and hooks, and a lateralfrontobasal burr hole is made using a high-speed drill. (D) After mobilization

of the dura mater, a straight line is cut in a lateral-to-medial direction, andthe craniotomy is then completed with a C-shaped incision. (E) An essentialstep of the approach is drilling of the inner edge of the bone above theorbital rim, increasing the angle for visualization and manipulation. (F) Thedura mater is opened simply in a curved way and retracted in a basaldirection, 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 usedmainly to visualize the target area beforeand after clipping and rarely for actualendoscope-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 allwith the microscope. In all cases, clipposition was subsequently corrected; themarkedly improved endoscopic visualiza-tion increased the likelihood of controllingideal aneurysmal closure.

Illustrative CaseA 33-year-old woman whose sister hadexperienced severe subarachnoid hemor-rhage underwent neurologic examinationthat included magnetic resonance imagingof the brain. Imaging detected bilateralaneurysms 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’sanxiety, the decision was made to treat theaneurysms. After performing digital sub-traction angiography and an interdisci-plinary discussion with the interventionalneuroradiologists concerning the treat-ment modality, surgical treatment waschosen. Factors favoring surgery were thesmall size of the left-sided aneurysm, theunfavorable aspect ratio of the dome andneck of the right-sided aneurysm, and thepatient’s request for surgical therapy(Figure 4A). Evaluation of magnetic reso-nance imaging and angiographic studiesincluding three-dimensional planningsoftware demonstrated that the left-sidedaneurysm was proximally located near theearly temporal branch. The right-sidedaneurysm originated more distally at theMCA bifurcation (Figure 5). A right-sidedsupraorbital subfrontal exposure waschosen, treating both aneurysms througha single minimally invasive approach.After performing the supraorbital

keyhole approach (Figure 3), the supra-sellar cisterns were opened, and thecontralateral internal carotid artery wasapproached (Figure 6A). Gentle retractionwas used; the elevator was placed betweenthe frontal lobe and olfactory nerve,avoiding stretching the fila olfactoria. Thecontralateral sylvian fissure was opened,approaching the left-sided aneurysm.

Endoscopic inspection verified the aneu-rysm neck and its relationship to the earlytemporal branch (Figure 6B). A straightbayonet-shaped clip was placed under

microscopic control, immediately closingthe aneurysm. The use of a tube-shaft clipapplier in the narrow corridor was crucial(Figure 6C). Complete aneurysm closure

Figure 4. (A) Preoperative angiography showing nonruptured bilateral aneurysms. The left-sidedmiddle cerebral artery aneurysm originates near the early temporal branch, and the right-sidedaneurysm originates at the middle cerebral artery bifurcation. (B) After surgery, digital subtractionangiography reveals no residual aneurysm.

Figure 5. (A) Three-dimensional observation of bilateral aneurysms demonstrating the relationship ofthe optic nerve and arterial vessels to the bony skull base structures allowing precise andcomprehensive surgical planning. (B) Virtual inspection through the right-sided keyhole craniotomyreveals that both aneurysms are safely approachable (Dextroscope; Volume Interactions, Singapore).

WORLD NEUROSURGERY 82 [6S]: S130-S137, DECEMBER 2014 www.WORLDNEUROSURGERY.org S133

PEER-REVIEW REPORTS

ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS

was controlled with the help of the endo-scope (Figure 6D). The right sylvian fissurewas opened without using the brainretractor. With microscopic visualization,the temporal branch of the MCA could notbe visualized behind the dome of theaneurysm (Figure 6E); however, this hid-den part of the field was ideally managedwith endoscopic assistance (Figure 6F).After successful clipping without the useof a retractor (Figure 6G), the clip positionwas endoscopically controlled, confirmingreliable aneurysm closure without nar-rowing the MCA bifurcation surroundingthe perforators (Figure 6H). Patency ofthe MCA branches was confirmed withDoppler sonography and indocyaninegreen angiography. Using the TEAMtechnique, both aneurysms could becompletely closed through the one-sidedlimited keyhole approach.The patient had an uneventful recovery.

Postoperative examination revealed noneurologic symptoms. computed tomog-raphy scan showed no intracranial com-plications and optimal repositioning ofthe bone flap. Cerebral angiographyshowed complete closure of both aneu-rysms (Figure 4B). The patient was able toreturn to her previous employment, andthe cosmetic result was excellent.

DISCUSSIONSince the beginning of neurosurgery, ithas been widely accepted that exposure ofbrain tissue for several hours during sur-gery using extended craniotomies resultsin injury of the cortical surface by non-physiologic surroundings, including roomair, irrigation, cover material, and spatulapressure (51). In addition, it has beenshown in many experimental and clinicalstudies that brain retraction causes sig-nificant intraoperative trauma to braintissue and may lead to permanent neuro-logic deficits (1, 2, 4, 25, 52). To minimizebrain retraction, various methods havebeen proposed (e.g., application of specialanesthetic techniques to achieve brainrelaxation, individual brain retractor sys-tems, unusual positioning techniques ofpatient) (12, 13, 16, 18, 50). However, thebest retraction is no retraction. Carefulchoice of an adequate, least invasive

Figure 6. Intraoperative photographs showing critical steps of the procedure. (A) First, the oppositeinternal carotid artery was approached, and the sylvian fissure was exposed. (B) The anatomy of theleft-sided aneurysm was investigated with the endoscope. After clipping with a tube-shaftinstrument, secured by safe proximal control (C), endoscopic control revealed complete occlusionwithout narrowing of the parent vessels (D). (E) Next, the right middle cerebral artery wasapproached, but the temporal branch could not be seen behind the aneurysm dome and sphenoidwing. With the endoscope, this hidden part could optimally be visualized (F), allowing safe clipapplication (G). (H) The last endoscopic investigation showed complete closure without tightening themiddle cerebral artery bifurcation. ICA, internal carotid artery; CN II, optic nerve; ETB, early temporalbranch; FB, frontal branch; TB, temporal branch.

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 brainexploration and dissection without the useof a retractor may result in a significantreduction of trauma to intracranial struc-tures (25, 37, 38).With the excellent diagnostic capabil-

ities of digital subtraction angiography,three-dimensional angiography,computed tomography, and MRI currentlyavailable, one can demonstrate and clarifythe individual spatial anatomy of a patientincluding the smallest details. Anatomi-cally suitable corridors for surgicaldissection can be described and discussedin a meticulous preoperative planningprocedure. With the knowledge of the in-dividual anatomic details of a specific pa-tient, it is possible to perform a tailoredsurgical procedure reducing the size of theskin incision, the craniotomy, and theextent of retraction and trauma to thebrain surface to a minimum. In recentyears, the ability to plan specific ap-proaches has been improved further byusing three-dimensional graphic tools ofradiologic image processing consoles orplanning software of surgical navigationsystems. We have also worked extensivelywith virtual reality environments, allowingprecise and comprehensive surgical plan-ning with multimodality, patient-specificthree-dimensional objects displayed in aspatial working environment (26, 43).The advantages of keyhole microsurgery

may contribute to improved postoperativeresults, including shorter hospitalizationtime because of reduction of the risk forcomplications, such as bleeding orrebleeding with neurologic deterioration,leakage of cerebrospinal fluid, infection,scarification, and cosmetic disturbances(37, 38). However, limited keyhole ap-proaches cause a significant loss of opticalcontrol, especially in the deep-seated sur-gical field. The first neurosurgeons whorealized the limitations of surgical micro-scopes and the advantages of endoscopicviews during microsurgical procedureswere Prott in 1974 (40), when he performedendoscopic cisternoscopy of the cer-ebellopontine angle; Apuzzo et al. in 1977(5), when they introduced the so-calledside-viewing telescope; and Oppel in 1981(34), when he applied intraoperativeendoscopy duringmicrovascular trigeminaldecompression. All of these descriptionscan be regarded as the initiation of endo-scope-assisted microneurosurgery, which,

along with other neuroendoscopic tech-niques, experienced an enormous revival inthe 1990s (11-13, 15, 19, 37, 39, 42). At thistime, Perneczky developed and refined theconcept of endoscopic and endoscope-assisted neurosurgery using limitedkeyhole approaches in transcranial neuro-surgery. As pioneer in minimal invasivetechniques, Perneczky became the teacherof countless residents and internationalfellows in the Neurosurgical Department ofthe University Mainz, Germany.The TEAM technique enables neuro-

surgeons to approach deep-seated regionsthrough narrow anatomic windows,without excessive retraction of sensitiveneurovascular structures. The endoscopicpictures allow illumination and inspectionof angles in hidden parts of the surgicalfield and, owing to the enormous opticaldepth of field of modern endoscopes,provide an almost three-dimensionalaspect of anatomic structures. Frequenttraining of spatial eye-hand coordination,which is necessary for all endoscope-assisted microsurgical procedures, enablesneurosurgeons to perform minimallyinvasive, maximally effective procedures.Rigid lens scopes are recommended for

endoscope-assisted microsurgery becauseonly the position of instruments with rigidshafts can be controlled precisely andbecause, at the present time, only lensscopes offer acceptable image quality. Inaddition, modern video and image pro-cessing technology with high-definitionvisualization is essential to achieve fullbenefit of endoscope-assisted microsur-gery (15, 42).

CONCLUSIONSThis article has provided a brief review ofour experience with the endoscope-assis-ted supraorbital keyhole approach in sur-gical treatment of intracranial aneurysms.This method allowed safe intraoperativecontrol of clipping of ruptured and inci-dental intracranial aneurysms. Because thelimited approach-related trauma to thebrain, postoperative results were favorablecompared with the results of interven-tional treatment. Essential prerequisites ofkeyhole aneurysm surgery are 1) carefulselection of cases, 2) accurate preoperativeplanning, 3) tailored placement of thecraniotomy, and 4) use of TEAM tech-niques. Intraoperative application of

endoscopes is mandatory for adequatevisualization, especially for control of clipplacement and assessment of surroundingperforators. In 19.1% of our cases,endoscopy revealed suboptimal clip posi-tion with residual neck, narrowed parentvessel, or occluded peforator that was notclearly detected with the microscope.Endoscopic visualization increased mark-edly the likelihood of controlling optimalaneurysmal closure and consequentlyachieving better surgical results.

ACKNOWLEDGMENTSTEAM technique involves real teamwork.We express our gratitude to our colleaguesin the Clinic Hirslanden Zurich; in theUniversity Hospitals Mainz, Homburg, andMannheim; and in the KatharinenhospitalStuttgart. Supraorbital craniotomy forintracranial aneurysms was first used anddescribed by our late teacher and mentor,Axel Perneczky. This article is dedicated tohim with deep grief and infinite respect.

REFERENCES1. Albin MS, Bunegin L, Dujovny M: Brain retraction

pressure during intracranial procedures. SurgForum 26:499-500, 1975.

2. Albin MS, Bunegin L, Bennett MH: Clinical andexperimental brain retraction pressure moni-toring. Acta Neurol Scand 65:522-523, 1977.

3. Andaluz N, Zuccarello M: Fenestration of thelamina terminalis as a valuable adjunct in aneu-rysm surgery. Neurosurgery 55:1050-1059, 2004.

4. Andrews RJ, Bringas JR: A review of brainretraction and recommendations for minimizingintraoperative brain injury. Neurosurgery 33:1052-1064, 1993.

5. Apuzzo ML, Heifetz MD, Weiss MH, Kurze T:Neurosurgical endoscopy using the side-viewingtelescope. Technical note. J Neurosurg 46:398-400, 1977.

6. Ausman JI: ISAT study: is coiling better thenclipping? Surg Neurol 59:162-165, 2003.

7. CohenAR, PerneczkyA,RodziewiczGS,Gingold SI:Endoscope-assisted craniotomy: approach to therostral brain stem. Neurosurgery 36:1128-1129, 1995.

8. Conrad MD, Pelissou-Guyotat I, Moral C,Madarassy G, Schonauer C, Deruty R: Regrowthof residual ruptured aneurysms treated byGuglielmi’s Detachable Coils which demandedfurther treatment by surgical clipping: report of 7cases and review of the literature. Acta Neurochir(Wien) 144:419-426, 2002.

9. Diringer MN: To clip or to coil acutely rupturedintracranial aneurysms: update on the debate.Curr Opin Crit Care 11:121-125, 2005.

WORLD NEUROSURGERY 82 [6S]: S130-S137, DECEMBER 2014 www.WORLDNEUROSURGERY.org S135

PEER-REVIEW REPORTS

ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS

10. Flett LM, Chandler CS, Giddings D, Gholkar A:Aneurysmal subarachnoid hemorrhage: manage-ment strategies and clinical outcomes in aregional neuroscience center. AJNR Am J Neuro-radiol 26:367-372, 2005.

11. Fischer G, Stadie A, Reisch R, Hopf NJ, Fries G,Böcher-Schwarz H, van Lindert E, Ungersböck K,Knosp E, Oertel J, Perneczky A: The keyholeconcept in aneurysm surgery: results of the past 20years. Neurosurgery 68:45-51, 2011.

12. Fries G, Perneczky A: Endoscope-assisted brainsurgery. Part 2—analysis of 380 procedures.Neurosurgery 42:226-232, 1998.

13. Fries G, Reisch R: Biportal neuroendoscopicmicrosurgical approaches to the subarachnoidcisterns: a cadaver study. Minim Invasive Neuro-surg 39:99-104, 1996.

14. Gorski R, Zabek M, Jarmuzek P: Influence ofintraoperative using of rt-PA on developmentof cerebral angiospasm after subarachnoidhemorrhage in patients with ruptures intracra-nial aneurysms. Neurol Neurochir Pol 34:41-47,2000.

15. Grotenhuis JA: Endoscope-Assisted Micro-neurosurgery. Nijmegen, The Netherlands:Machaon; 1998.

16. Hasegawa T, Yamano K, Miyamori T:A micromanipulator for precise control of brainretractor. Technical note. J Neurosurg 74:1009-1010, 1991.

17. Hirashima Y, Hamada H, Hayashi N,Kuwayama N, Origasa H, Endo S: Independentpredictors of late hydrocephalus in patients withaneurysmal subarachnoid hemorrhage—analysisby multivariate logistic regression model. Cere-brovasc Dis 16:205-210, 2003.

18. Hongo K, Kobayashi S, Yokoh A: Monitoringretraction pressure on the brain. An experi-mental and clinical study. J Neurosurg 66:270-275, 1987.

19. Hopf NJ, Stadie A, Reisch R: Surgical manage-ment of bilateral middle cerebral artery aneu-rysms via a unilateral supraorbital key-holecraniotomy. Minim Invasive Neurosurg 52:126-131, 2009.

20. Hosoda K, Fujita S, Kawaguchi T, Shose Y,Hamano S, Iwakura M: Effect of clot removal andsurgical manipulation on regional cerebral bloodflow and delayed vasospasm in early aneurysmsurgery for subarachnoidal hemorrhage. SurgNeurol 51:81-88, 1999.

21. Inagawa T, Ohbayashi N, Kumano K: Effect ofrapid spontaneous diminution of subarachnoidhemorrhage on cerebral vasopasm. Surg Neurol43:25-30, 1995.

22. Inagawa T, Yamamoto M, Kamiya K: Effect of clotremoval on cerebral vasopasm. J Neurosurg 72:224-230, 1990.

23. Kalavakonda C, Sekhar LN, Ramachandran P,Hechl P: Endoscope-assisted microneurosurgery

for intracranial aneurysms. Neurosurgery 51:1119-1126, 2002.

24. Kasuya H, Shimizu T, Kagawa M: The effect ofcontinuous drainage of cerebrospinal fluid inpatients with subarachnoid hemorrhage: a retro-spective analysis of 108 patients. Neurosurgery 18:56-59, 1991.

25. Kivisaari RP, Salonen O, Ohman J: Basal braininjury in aneurysm surgery. Neurosurgery 46:1070-1074, 2000.

26. Kockro RA, Stadie A, Schwandt E, Reisch R,Charalampaki C, Ng I, Yeo TT, Hwang P, Serra L,Perneczky A: A collaborative virtual reality envi-ronment for neurosurgical planning and training.Neurosurgery 61:379-391, 2007.

27. Komotar RJ, Olivi A, Rigamonti D,Tamargo RJ: Microsurgical fenestration of thelamina terminalis reduces the incidence ofshunt-dependent hydrocephalus after aneu-rysmal subarachnoid hemorrhage. Neurosurgery51:1403-1412, 2002.

28. Lindsay KW: The impact of the InternationalSubarachnoid Aneurysm Trial (ISAT) on neuro-surgical practice. Acta Neurochir (Wien) 145:97-99, 2003.

29. MacDonald RL,WallaceMC, Coyne TJ: The effect ofsurgery on severity of vasospasm. J Neurosurg 80:433-439, 1994.

30. Menovsky T, Grotenhuis JA, de Vries J,Bartels RH: Endoscope-assisted supraorbitalcraniotomy for lesions of the interpeduncularfossa. Neurosurgery 44:106-110, 1999.

31. Molyneux A, Kerr R, Stratton I, Sanderock P,Clarke M, Shrimpton J, Holman R; ISAT Collab-orative Group: International Subarachnoid Aneu-rysm Trial (ISAT) of neurosurgical clipping versusendovascular coiling in 2143 patients withruptured intracranial aneurysms: a randomizedtrial. Lancet 360:1267-1274, 2002.

32. Niemela M, Koivisto T, Kivipelto L, Ishii K,Rinne J, Ronkainen A, Kivisaari R, Shen H,Karatas A, Lehecka M, Frosen J, Piippo A,Jaaskelainen J, Hernesniemi J: Microsurgical clip-ping of cerebral aneurysms after the ISAT study.Acta Neurochir Suppl 94:3-6, 2005.

33. Ogilvy CS, Hoh BL, Singer RJ, Putman CM: Clin-ical and radiographic outcome in the managementof posterior circulation aneurysms by use of directsurgical or endovascular techniques. Neurosurgery51:14-21, 2002.

34. Oppel F: Indications and operative technique forendoscopy of the cerebellopontine angle. In:Samii M, Jannetta P, eds. The Cranial Nerves.Berlin: Springer; 1981:429-437.

35. Perneczky A: Planning strategies for the supra-sellar region. Neurosurgeons 11:343-348, 1992.

36. Perneczky A, Fries G: Use of a new aneurysm clipwith inverted-spring mechanism to facilitate vi-sual control during clip application. Technicalnote. J Neurosurg 82:898-899, 1995.

37. Perneczky A, Fries G: Endoscope-assisted brainsurgery. Part 1—evolution, basic concept andcurrent technique. Neurosurgery 42:219-225,1998.

38. Perneczky A, Müller-Forell W, van Lindert E,Fries G: Keyhole Concept in Neurosurgery. Stutt-gart: Thieme Verlag; 1998.

39. Perneczky A, Reisch R: Key Hole Approaches inNeurosurgery. Volume I, Concept and SurgicalTechnique. Vienna: Springer Verlag; 2008.

40. Prott W: Cisternoscopy-endoscopy of the cer-ebellopontine angle. Acta Neurochir 1:105-113,1974.

41. Reisch R, Fries G, Patonay L, Perneczky A:Biportal neuroendoscopy of the prepontinecisterns [in Hungarian]. Ideggyogy Sz 56:76-81,2003.

42. Reisch R, Stadie A, Kockro R, Gawish I,Schwandt E, Hopf N: The minimally invasivesupraorbital subfrontal key-hole approach forsurgical treatment of temporomesial lesions ofthe dominant hemisphere. Minim InvasiveNeurosurg 52:163-169, 2009.

43. Stoodley M, MacDonald RL, Weir B, Marton LS,Johns L, Du Zhang Z, Kowalczuk A: Subarach-noid hemorrhage as a cause of an adaptiveresponse in cerebral arteries. J Neurosurg 93:463-470, 2000.

44. Stadie AT, Kockro RA, Reisch R, Tropine A,Boor S, Stoeter P, Perneczky A: Virtual realitysystem for planning minimally invasive neuro-surgery. Technical note. J Neurosurg 108:382-394,2008.

45. Tomasello F, d’Avella D, de Divitiis O: Doeslamina terminalis fenestration reduce the inci-dence of chronic hydrocephalus after subarach-noid hemorrhage? Neurosurgery 45:827-831,1999.

46. Tomasello F, d’Avella D: Intracisternal rt-PAduring early surgery for aneurismal subarachnoidhemorrhage: an Italian report. J Neurosurg Sci 37:71-75, 1993.

47. Tsuji T, Cook DA, Weir BK, Handa Y: Effect ofclot removal on cerebrovascular contractionafter subarachnoid hemorrhage in the monkey:pharmacological study. Heat Vessels 11:69-79,1996.

48. Van den Berg R, Rinkel GJ, Vandertop WP:Treatment of ruptured intracranial aneurysms:implications of the ISAT in clipping versus coil-ing. Eur J Radiol 46:172-177, 2003.

49. Van Lindert E, Perneczky A, Fries G, Pierangeli E:The supraorbital keyhole approach to supra-tentorial aneurysms. Concept and technique. SurgNeurol 49:481-490, 1999.

50. Waring AJ, Housworth CM, Voorhies RM:A prototype retractor system designed tominimize ischemic brain retractor injury. Anexperimental study. J Neurosurg 58:139-143,1990.

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-surgery. Technical note. J Neurosurg 34:102-106,1971.

52. Yokoh A, Sugita K, Kobayashi S: Clinical study ofbrain retraction in different approaches and dis-eases. Acta Neurochir 87:134-139, 1987.

53. Zhang ZD, Yamini B, Komuro T, Ono S, Johns L,Marton LS, Weir B, MacDonald RL: Vasospasm in

monkeys resolves because of loss of and encase-ment of subarachnoid blood clot. Stroke 32:1868-1874, 2001.

Conflict of interest statement: The authors declare that thearticle content was composed in the absence of anycommercial or financial relationships that could be construedas a potential conflict of interest.

Received 19 September 2013; accepted 25 July 2014

Citation: World Neurosurg. (2014) 82, 6S:S130-S137.http://dx.doi.org/10.1016/j.wneu.2014.07.038

Journal homepage: www.WORLDNEUROSURGERY.org

Available online: www.sciencedirect.com

1878-8750/$ - see front matter ª 2014 Published by ElsevierInc.

WORLD NEUROSURGERY 82 [6S]: S130-S137, DECEMBER 2014 www.WORLDNEUROSURGERY.org S137

PEER-REVIEW REPORTS

ROBERT REISCH ET AL. SUPRAORBITAL ENDOSCOPIC APPROACH FOR ANEURYSMS