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PEER-REVIEW REPORTS

Minimally Invasive Supracondylar Transtubercular (MIST) Approach to theLower Clivus

Vittorio M. Russo1,2, Francesca Graziano1,2, Monica Quiroga3, Antonino Russo2, Erminia Albanese2, Arthur J. Ulm1

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INTRODUCTION

The far-lateral approach (FLA), consistingof a lateral suboccipital craniotomy with re-moval of the C1 arch (Figures 1 and 2), hasbeen the primary surgical approach used toaccess lesions involving the inferior clivus,pontomedullary junction, lateral medulla,vertebrobasilar junction (VBJ) and postero-inferior cerebellar artery (PICA; 2, 5, 10-12,14, 15, 21, 22, 24, 27, 28, 31). Depending onthe localization of the lesion and the ana-tomic characteristics of the surroundingstructures, the surgeon may be required toperform a vascular transposition of the ver-tebral artery or to further drill osseous ob-stacles, in order to extend the exposure ofthe basic FLA. The transcondylar extension

Key words� Clivus� Endoscope-assisted surgery� Far-lateral approach� Jugular tubercle� Microsurgical anatomy� Supracondylar transtubercular approach

Abbreviations and AcronymsCN: Cranial nerveFLA: Far-lateral approachJT: Jugular tubercleMIST: Minimally invasive supracondylartranstubercularPICA: Posteroinferior cerebellar arteryVA: Vertebral arteryVB: VertebrobasilarVBJ: Vertebrobasilar junction

From the 1Departmentof Neurosurgery,

Louisiana State University, New Orleans, Louisiana, USA;2Department of Neurosurgery, University of Catania, Italy;nd 3Department of Neurosurgery, University of Costa Rica,an Josè, Costa Rica

o whom correspondence should be addressed:ittorio M. Russo, M.D. [E-mail: vichanit@yahoo.it]

itation: World Neurosurg. (2012) 77, 5/6:704-712.OI: 10.1016/j.wneu.2011.03.024

ournal homepage: www.WORLDNEUROSURGERY.org

vailable online: www.sciencedirect.com

878-8750/$ - see front matter © 2012 Elsevier Inc.ll rights reserved.

involves the extradural removal of the pos- w

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erior third of the occipital condyle (Figuresand 2). Further exposure can be achievedy removing the jugular tubercle (JT), whichignificantly improves access to the anterolat-ral brainstem and the structures located inhe premedullary cisterns (Figures 1 and 2).rawbacks to the extended FLAs include theorbidity of a large incision extending into

he upper cervical spine, the exposure andanipulation of the horizontal V3 segment of

he vertebral artery (VA), and operative time.

ETHODS

total of 10 cadaveric specimens (20 sides)

� OBJECTIVE: Drawbacks of the far-pontomedullary region include the mothe cervical musculature and tediouparticularly when performing the tranThe authors describe a minimally invathat has the potential to minimize operVA manipulation.

� METHODS: The minimally invasivear-lateral supracondylar transtubercu0 adult cadaveric specimens (20 sidesnd the surgical views were analyzediew through the MIST was examineides).

RESULTS: The MIST approach provithe anterolateral brainstem, and thPICA-VA and vertebrobasilar junctionscranial nerves III through XII, as wellapproach increased visualization ofmagnum; otherwise, the surgical viewapproaches.

� CONCLUSIONS: The MIST approaalternative to the FLST approach in theand middle clivus, and anterolateral llaminectomy, significant disruption ofexposure of the extracranial VA. Mocompanion to endoscope-assisted neu

ere included in this study. The arteries and b

WORLD NEUROSURGE

eins were infused with colored silicone.sing �3 to �40 magnification, the micro-

urgical anatomy was examined bilaterallyhile performing the minimally invasive

upracondylar transtubercular (MIST) ap-roach and the far-lateral supracondylar tr-nstubercular approach. In addition, thendoscopic view through the MIST was ex-mined in five fresh cadaveric specimens10 sides) using a rigid endoscope.

IST Surgical Techniquepecimens were dissected in a manner toimulate patient positioning in a Park

al approach to the lower clivus andity of a large incision extending intoposure of the vertebral artery (VA),dylar and transtubercular extensions.alternative to the far-lateral approach

morbidity and decrease the need for

acondylar transtubercular (MIST) andFLST) approaches were performed ine microsurgical anatomy of each step

compared. In addition, the endoscopicfive fresh cadaveric specimens (10

exposure of the inferior-middle clivus,remedullary cisterns, including the

endoscope provided a clear view ofthe vertebrobasilar system. The FLSTanterolateral margin of the foramensimilar between the MIST and FLST

ould be considered as a potentialtment of lesions involving the inferiorr brainstem; it does not require a C1atlanto-occipital joint, nor extensive

ver, the MIST approach is an idealrgery.

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Figure 1. (A) Far-lateral approach and its extensions. A large hockey-stickor paramedian straight skin incision, extending into the upper cervicalspine, is commonly selected for the far-lateral exposure (insert). In thiscadaveric dissection, the muscles forming the margins of the suboccipitaltriangle have been removed to show the vertebral artery and the C2nerve exiting between the C1 and C2 laminas. The vertical part and thedistal loop of the V3 segment of the vertebral artery are exposed. Thehorizontal segment of V3 occupies the groove of the posterior arch of theatlas and pierces the dura just medial to the condyle. Before drilling, thissegment of the vertebral artery must be identified in order to preventiatrogenic vascular injury. Classic far-lateral craniotomy (green-coloredarea) includes the resection of the C1 hemilamina. The transcondylarapproach includes drilling of the posterior third of the occipital condyleuntil reaching the posterior wall of the hypoglossal canal (oblique reddotted lines). The supracondylar transtubercular extension of the approach(yellow dotted lines) involves drilling through the condylar fossa and thejugular tubercle. (B) Minimally invasive supracondylar transtubercular(MIST) approach. A small vertical or slightly S-shaped skin incision,centered approximately 2 cm medial to the mastoid process is chosenwhen performing the MIST approach (insert). A small lateral suboccipitalcraniotomy (green-colored area) is required; it includes the resection ofthe posterolateral rim of the foramen magnum and extends laterally untilthe medial edge of the sigmoid sinus. A small portion of the superior–posterior–medial edge of the occipital condyle is resected with minimaljoint disruption. Next, the condylar fossa is drilled from superficial to deepin order to remove the jugular tubercle (red dotted line). (C) Lateralsuboccipital craniotomy includes resection of the posterolateral rim of theoccipital foramen and extends laterally until the medial border of thesigmoid sinus. Any bony impedance medial to the sigmoid sinus andoccipital condyle is removed with a shaving burr. (D) Posteroinferior viewof the occipital bone and foramen magnum. In the MIST approach, bonyremoval includes also a partial resection of the most superior–posterior–medial edge of the occipital condyle, and drilling of the condylar fossaabove the condyle (red dotted lines). Most of the occipital condyle is leftintact. (E and F) Supracondylar and transcondylar extensions of the far-lateral approach. (E) Posteroinferior view of the occipital bone andforamen magnum. The supracondylar approach includes drilling throughthe condylar fossa (yellow dotted lines). The condylar fossa is adepression located on the external surface of the occipital bone, behindthe occipital condyle; there is often an emissary vein and associatedposterior condylar canal through which the posterior condylar veinconnects the vertebral artery venous plexus to the sigmoid sinus. Thecondylar fossa lies superficial to the jugular tubercle and lies between thejugular bulb laterally and the posterolateral portion of the foramenmagnum medially. The transcondylar approach involves drilling of theposterior third of the occipital condyle. The soft cancellous bone of thecondyle is removed until reaching the cortical bone that forms the

posterior wall of the hypoglossal canal. (F) Medial view of the occipital condyle, intracranial opening of hypoglossal canal and jugular tubercle. The posterior third of the occipital condyle is removeduntil reaching the posterior margin of the hypoglossal canal, during the transcondylar approach (black dotted lines). The yellow dotted lines indicate the supracondylar drilling through the condylarfossa, above the occipital condyle and hypoglossal canal and extending anteriorly through the jugular tubercle. A., artery; Atl., atlanto-; Cap., capitis; Cond., condyle; Dig., digastric; For., foramen;Hypogl., hypoglossal; Jug., jugular; Lat., lateralis; M., muscle; Occip., occipital; Proc., process; Rec., rectus; Sig., sigmoid ; Trans., transverse; Tub., tubercle; Vert., vertebral.

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PEER-REVIEW REPORTS

VITTORIO M. RUSSO ET AL. MIST APPROACH TO THE LOWER CLIVUS

adequate flexion of the neck to open theipsilateral craniovertebral junction. A5-cm vertical, or slightly S-shaped, skinincision was made, centered approxi-mately 2 cm medial to the mastoid pro-cess (Figure 1). The suboccipital muscleswere dissected and separated from theirattachment to the bone. A small, lateralsuboccipital craniotomy was performed,including resection of the posterolateralrim of the foramen magnum and extend-ing laterally until the medial edge of thesigmoid sinus. Inferiorly and laterally,the craniotomy was extended with a shav-ing burr, over the condylar fossa and con-dylar canal to remove any bony impedancemedial to the sigmoid sinus and occipitalcondyle (Figure 1). Condylar removal waslimited to the upper medial posterior as-pect. Access to the condyle was obtainedby opening the superior-medial attach-ment of the joint capsule and depressing

Figure 2. Intradural view of the far-lateralapproach, transcondylar and supracondylarextensions. (A) The lateral suboccipitalcraniotomy has been performed and C1 laminaremoved from the midline to the sulcusarteriosus. The dura mater has been openedand retracted laterally while the cerebellartonsil is gently retracted upward and medially.The glossopharyngeal, vagus, and accessorynerve arise from the posterior margin of theolive and ascend to reach the jugular foramen.The hypoglossal nerve arises along the front ofthe inferior olive anterior to the origin of thecranial accessory fibers as a series of rootlets thdural orifice of the hypoglossal canal. At its origibetween, the hypoglossal rootlets. (B) The transbeen performed. The removal of the posterior ththe dura mater provides a wider exposure of thelateral to medial and caudo-cranial view, the antbrainstem are visualized. At this stage, the prombasilar cisterns and lower clivus. (C) Drilling hasthe jugular tubercle has been removed extradurathe space created by the removal of this bone.X complex and CN XI is gained. Also, a greaterlower clivus. A., artery; Atl., atlanto-; CN., craniahypoglossal; Jug., jugular; Lig., ligament; N., nercerebellar artery; Vert., vertebral.

the capsule inferiorly. The capsule was t

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90% intact after resection (Figure 1).ony removal included the drilling of the con-ylar fossa above the condyle to expose theoof of the hypoglossal canal (Figures 1 and). After exposing the roof of the hypoglossalanal, the extradural resection of the JT fol-owed; the overlying dura was first separatedrom the tubercle and then the drilling wasontinued through the cancellous bone abovehe hypoglossal canal, medial to the jugularulb, in a superoanteromedial direction ap-roximately 45 degrees in the sagittal planeFigure 3). The softer cancellous bone wasrilled out first and then the harder corti-al edges were thinned out and removedith a fine dissector. After performing the

uberculectomy, the dura was openedith a curvilinear incision extending me-ial to the sigmoid sinus, over the cere-ellar surface, and then inferiorly and me-ial to the VA dural entry point, based

s behind the vertebral artery as they enter thePICA may pass rostral or caudal to, orlar extension of the far-lateral approach hasthe occipital condyle and lateral retraction of

al pontomedullary junction region. With a moreral portion of the foramen magnum ande of the jugular tubercle blocks access to theextended through the condylar fossa ande dura mater has been retracted laterally intoreased visualization between the CN IX and CNg space is created when approaching the

e; Dent., dentate; For., foramen; Hypogl.,ccip., occipital; P.I.C.A., posterior inferior

oward the sinus and occipital condyle. a

WORLD NEUROSURGE

djunctive Endoscopyn the fresh cadaveric specimens we per-ormed the MIST approach; after an initialxamination of intradural anatomic struc-ures under the operating microscope, aigid endoscope was introduced and guidednto position. The endoscope was intro-uced through three different surgical cor-idors. The diameter of the endoscope was.7 mm, with an angulation of 30 degreesStryker; San Jose, California, USA). Ahree-chip digital camera (1188 HD, 5900ptical Court, Stryker) was attached to the

ndoscope; illumination was provided withxenon light source (X8000, Stryker). The

ideo images were displayed on a videoonitor (Vision Elect HD TV, Stryker) and

tored with a digital capture device (SDCD, Stryker).

ESULTS

natomic Considerationshe relationship of the anatomic structuresust be considered when performing the

xtradural resection of the JT, in order tovoid neural or vascular injuries. The JT isocated at the junction of the basilar andondylar portions of the occipital bone. Inur cadaveric dissection, the mean distancerom the posterior border of the intracranialpening of the hypoglossal canal to thepex of the JT was 14.0 � 2 mm; the meanistance from the JT apex to the posterome-ial edge of the occipital condyle was 25.9 �.2 mm.

At the beginning of the tuberculec-omy, drilling takes place between the in-racranial openings of the hypoglossal ca-al and jugular foramen, at the base of the

T (Figure 3); in our specimens, the dis-ance between these two foramens aver-ged 10.2 � 1.0 mm. While drilling alonghe posteromedial edge of the condyle,he intracranial opening of the hypoglos-al canal was located at a depth of approx-mately 9.8 � 2.5 mm. The hypoglossalanal venous plexus occupied most of theanal, especially on the cephalic and pos-erior parts (Figure 3), providing a safentry zone into the canal.

It is important to note that the acces-ory nerve, as well as rootlets of the IX andcranial nerves, travels on the dura over-

ying the base of the JT (Figure 3); there-ore, drilling of the tubercle should

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RY, DOI:10.1016/j.wneu.2011.03.024

PEER-REVIEW REPORTS

VITTORIO M. RUSSO ET AL. MIST APPROACH TO THE LOWER CLIVUS

WORL

Figure 3. Minimally invasive supracondylar transtubercular approach.Condylar fossa drilling, jugular tuberculectomy, and hypoglossal canalanatomy. (A) The dura has been cut parallel to the spinal accessory nerveto show its relationship with the base of the jugular tubercle. During theminimally invasive supracondylar transtubercular approach, extraduraldrilling is begun at the most posteromedial edge of the occipital condylewithout disrupting the articular cartilage, in an anterosuperior direction,parallel and lateral to the veins that communicate the perivertebral venousplexus and the hypoglossal canal venous plexus. The drilling is maintainedmedial to the posterior emmisary and condylar vein and canal, betweenthe intracranial openings of the hypoglossal and jugular foramens (insert).(B) Upward retraction of the cerebellar tonsil allows visualization of thejugular tubercle (starred) as it projects anterior to the glossopharyngeal,vagus, and accessory nerves. When drilling the jugular tubercle, irrigationis very important to prevent thermal injury to the accessory nerve, whichtravels just above the overlying dura of the jugular tubercle. Also, theglossopharyngeal and vagus nerves may be injured if the dura isperforated either by the drill or the dissector. (C) The cancellous boneover the cortical bone of the hypoglossal canal has been removed.Venous extensions from the hypoglossal canal may project through theroof of the canal. The jugular tubercle is resected extradurally bycontinuing further drilling in an anteromedial direction. (D) The roof andposterior wall of the medial part of the hypoglossal canal have beenremoved and the venous plexus of the canal is encountered. Beneath this vein, the hypoglossal nerve bundles travel inside the canal divided in thisspecimen by a bony septum (starred). A meningeal branch of the ascending pharyngeal artery also travels inside the canal. (E) The venous plexus of thehypoglossal canal has been removed and the cancellous bone (starred) of the jugular tubercle can be seen anterior and superior to the canal. A., artery;Atl., atlanto-; Asc., ascending; Br., branch; CN., cranial nerve; Can., canal; Cond., condyle; Emiss., emissary; Ext., external; Men., meningeal; Occip.,occipital; Occipitomast., occipitomastoid; Pharyn., pharyngeal; P.I.C.A., posteroinferior cerebellar artery; Plex., plexus; Post., posterior; V., vein; Vert.,

vertebral.

D NEUROSURGERY 77 [5/6]: 704-712, MAY/JUNE 2012 www.WORLDNEUROSURGERY.org 707

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PEER-REVIEW REPORTS

VITTORIO M. RUSSO ET AL. MIST APPROACH TO THE LOWER CLIVUS

gation in order to prevent thermal injuryto those nerves. The accessory nerve, aswell as the glossopharyngeal and vagus,may also be injured if the dura is perfo-rated either with the drill or with a dissec-tor. Anterior to the JT, the anteroinferiorcerebellar artery was frequently foundcoursing laterally away from the basilarartery, so care must be taken when dril-ling the anterior part of the tubercle so asto avoid injury to this vessel. When theintradural VA was found to be tortuous oraccompanied by a high VBJ, the VA couldbe found in proximity to the inferomedialedge of the tubercle. Similarly, the lateralmedullary segment of the PICA can form alateral loop that may extend out closeto the JT (25) (Figure 3). Also, if drilling atthe base of the JT is extended too laterally,the jugular bulb may be disrupted and, ifit is performed too anterolaterally, the in-ferior petrosal sinus may be injured aswell.

Special care must be taken when open-ing the dura around the VA since the PICAor posterior spinal artery may originate ormay travel close to that site (26). Once thedura is opened, the accessory nerve is thefirst cranial nerve to come into view (Fig-

Figure 4. Intradural course of the hypoglossal nernerve extends from the preolivary sulcus (arrowusually travelling over the vertebral artery, throuhypoglossal canal, the nerve is accompanied byartery and a venous plexus, the anterior condylaanatomic studies, the rootlets of the hypoglossaA., artery; Atl., atlanto-; CN., cranial nerve; OccipVert., vertebral.

ure 3). The rootlets of the accessory nerve n

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rise from the postolivary sulcus and joino form a compact nerve bundle that trav-ls close or adjacent to the dura beforentering the jugular foramen. Anterior tohe spinal accessory nerve, the dentateigament is found with its two rostral ex-ensions wrapping around the VA. Theentate ligament is paler than the neigh-oring nerves, extends in a sheet-likeashion from the lateral spinal cord to-ard the lateral dura and attaching as twobrous strands rostrally. The strand ofentate ligament located between the spi-al accessory nerve and the VA may be

ransected and also retracted, allowingetter mobilization of the VA and improv-

ng the working space between the me-ulla oblongata and the VA when treatingBJ aneurysms or anterior foramen mag-um tumors (3, 11, 13). The cisternal seg-ent of the hypoglossal nerve exits from

he preolivary sulcus of the medulla in theorm of various rootlets (Figure 4). Theseroject laterally across the premedullaryistern, passing usually over the vertebralrtery and entering the hypoglossal canalFigure 4). In our specimens, as well as inrevious anatomic studies, the rootletsost frequently enter the hypoglossal ca-

d its vascular relationship. (A) The hypoglossale intracranial opening of the hypoglossal canal,premedullary cistern. (B) Inside the

ningeal branch of the ascending pharyngeal. In this specimen, as well as in previouse enter the canal in the form of two bundles.ipital; P.I.C.A., posteroinferior cerebellar artery;

al in the form of two bundles (Figures 3 e

WORLD NEUROSURGE

nd 4) (1, 4). The intracranial opening ofhe hypoglossal canal is located just abovehe occipital condyle, usually in the areahere the posterior and middle thirds of

he condyle meet. The hypoglossal canalxtends in an anterolateral direction, andxits at the level of the anterior and mid-le thirds of the condyle. In addition to

he hypoglossal nerve, the hypoglossalanal contains a venous plexus, alsoamed the anterior condylar vein and aeningeal branch from the ascending

haryngeal artery (Figures 3 and 4). Arimitive hypoglossal artery may also tra-erse the canal. In our dissections, a bonyeptum located most frequently at the me-ial end, divided the hypoglossal canal in0% of specimens (Figure 3). In anothernatomic study, this septum was found in8% of dissections (4). Each hypoglossalerve bundle usually travels within theiddle or inferior third of each canal.hen a prominent meningeal artery is

resent, it usually travels between or onop of the bundles. When a bony septums present, this artery will usually travel inhe most posterior subcanal (1, 7).

The extradural drilling performed in theIST approach, including the tuberculec-

omy, provides a posterolateral to medial sur-ical view. There is increased visualization of

he intradural VA, the PICA–VA junction, theBJ and the proximal basilar artery with itserforating branches, the anteroinferior cere-ellar artery and, in some cases, also the laby-inthine artery (Figure 5). With a more lateralo medial view, the anterolateral surface of therainstem may be visualized, including thelive with the adjoining rootlets of the inferiorranial nerves. With a more superior viewingngle, the cisternal segment of the abducenserve may be observed. With a more anterioriew, the inferior and middle clivus are seen.

ndoscope-Assisted MIST Approachn five fresh specimens, the adjunctive useful-ess of the endoscope was assessed. Threeistinct working views and trajectories wereossible after performing the MIST approachFigure 6). The removal of the JT allowed theateral retraction of the overlying dura androvided an enlarged corridor through which

he endoscope could be advanced, lateral toedial, toward the lower third of the clivus,

etween cranial nerve (CN) XI and the rootletsf CN IX. With an inferomedial trajectory, lat-

ve an) to thgh thea mer veinl nerv., occ

ral to the medulla, below CN IX, the anterior

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PEER-REVIEW REPORTS

VITTORIO M. RUSSO ET AL. MIST APPROACH TO THE LOWER CLIVUS

craniovertebral junction was clearly visual-ized. With superior medial retraction of thetonsils and lower lateral cerebellum, the en-doscope was advanced above CN X, just in-ferolateral to the flocculus, allowing visual-ization of the cerebellopontine angle(Figure 6).

DISCUSSION

Far-lateral craniotomy has been the pri-mary surgical approach used to access le-sions involving the inferior clivus, pon-

Figure 5. Surgical view before and after the resetuberculectomy performed in the minimally invathe surgeon a posterolateral to medial surgical vvertebral artery (VA), posteroinferior cerebellar aand the proximal basilar artery with its perforatin(AICA), and in some cases, also the labyrinthineview of the basilar artery and the mid-lower clivespecially of the basilar artery, AICA, and middle(C) Enlarged view of the vertebrobasilar junctionmore lateral to medial and a slightly inferior to sartery and PICA–VA junction (arrow) could be obPICA passes between the rootlets of the hypogmedulla. A., artery; A.I.C.A., anteroinferior cerebposteroinferior cerebellar artery; Vert., vertebral.

tomedullary junction, lateral medulla, V

WORLD NEUROSURGERY 77 [5/6]: 704-7

BJ, and PICA (Figures 1 and 2) (2, 5,0-12, 14, 15, 18, 21, 22, 24, 27, 28, 31).he surgical exposure of the far-lateralan be extended by removing the poste-ior third of the occipital condyle to im-rove access to the lateral medulla (Fig-res 1 and 2) and further extended withhe additional removal of the JT to im-rove access to the anteroinferior clivusFigures 1 and 2). The major drawbacks ofhe procedure include a large skin inci-ion extending into the upper cervicalpine, tedious exposure of the horizontal

f the jugular tubercle. The extraduralupracondylar transtubercular approach giveshere is increased visualization of the intraduralPICA)–VA junction, vertebrobasilar junction,nches, the anteroinferior cerebellar artery. (A) The jugular tubercle (starred) narrows the

) After tuberculectomy, there is increased viewal part of the middle and lower clivus (starred).rigin of AICA. (D) After tuberculectomy, with ar view, the intradural portion of the vertebrald. After its origin near the inferior olive, thenerve, at the anterolateral margin of thertery; Bas., basilar; CN., cranial nerve; P.I.C.A.,

3 segment, as well as potential atlanto-

12, MAY/JUNE 2012 ww

ccipital instability as a result of the dis-uption of the occipitocervical joint asso-iated with wide removal of the occipitalondyle (29).

The MIST approach (Figures 1 and 5) rep-resents an alternative to the standard FLA tothe lower clivus and pontomedullary re-gion. The approach has the potential tominimize operative morbidity, without sac-rificing surgical exposure, when applied toproperly selected pathology. Potential ad-vantages include a smaller skin incision, lo-calized suboccipital craniotomy, and no re-moval or exposure of the C1 arch. Limitedresection of the occipital condyle coupledwith an extradural resection of the JT pro-vides access to the lower clivus without theneed for extensive VA exposure and manip-ulation and with minimal risk of occipito-cervical instability.

With the traditional transcondylar ex-tension of the FLA, a large portion of thejoint capsule is removed and the condyleis drilled out anteriorly to the hypoglossalcanal. This level of drilling correspondsto the resection of approximately the pos-terior third of the condyle (Figure 1).However, it is often difficult to preciselylocalize the intradural hypoglossal canalwhen removing the condyle via extraduraldrilling, and this can result in a more ex-tensive condyle resection. Previous re-ports have suggested a high rate of insta-bility with �50% resection of theoccipital condyle (29). In the MIST ap-proach, the majority of the capsule re-mains intact, with only disruption of thesuperior medial aspect, and drilling isconfined to much less than the third of thecondyle (Figure 1).

Visualization of the lower clivus is ob-structed by the JT when approaching theregion through the suboccipital and the far-lateral approaches (Figures 2 and 7). By re-moving the JT extradurally, a corridor is cre-ated above CN XI and below CN IX and CNX. The dura can be retracted into the spacecreated by the removal of this bone, whichincreases visualization medially betweenthe CN IX and CN X complexes and CN XI.In addition, the bony removal provides anenlarged surgical view and increases work-ing space when approaching the lower cli-vus (Figures 2 and 5).

We compared the exposure between theextended far-lateral (Figures 1 and 2)

ction osive siew. Trtery (g braartery

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PEER-REVIEW REPORTS

VITTORIO M. RUSSO ET AL. MIST APPROACH TO THE LOWER CLIVUS

arch, removal of the posterior third of theoccipital condyle, and JT resection) andthe MIST approaches (Figures 1 and 5,Table 1). The exposure of the lateral me-dulla and lower clivus were identical be-tween the approaches. The extended far-lateral provided increased exposure of thedorsal and anterolateral foramen mag-num but not of the lateral medulla andlower third of the clivus.

The usefulness of endoscopic tech-niques as an adjunctive tool during micro-

Figure 6. Endoscope-assisted minimally invasive suWith an inferomedial trajectory (blue arrow) lateralCN IX to visualize the anterior craniovertebral junctby the resection of the jugular tubercle, enclosedinferiorly, and the glossopharyngeal and vagus nerthe tonsils and lower lateral cerebellum, the endosthe flocculus. (D) Panoramic view of the vertebraltrunk, and the proximal segment of AICA. Also, thmargin of the pons. (E) Moving the endoscope forappreciate the trigeminal nerve entering the porusthe Dorello canal, in correspondence to the posterthe lateral pontomesencephalic segment of the suruns just close to the trigeminal nerve; the trochleabove the midportion of this segment. The oculomartery (PCA) and the SCA. (F) Close-up view of thevestibulocochlear nerves medially. The latter ariseanteriorly to the flocculus and to the choroid plexuis visualized. The facial and vestibulocochlear nervnerve entering the trigeminal porus is observed. Acerebral artery; P.I.C.A., posteroinferior cerebellar

surgical approaches to the posterior fossa

710 www.SCIENCEDIRECT.com

and cerebellopontine angle has been re-ported for the treatment of acoustic neu-romas, intrinsic and extrinsic lesions in-volving the brainstem, microvasculardecompression of the cranial nerves, andaneurysms of the vertebrobasilar system(8, 9, 16, 17, 23, 30). In this study, we havedemonstrated that the MIST approach isan ideal companion to endoscope-as-sisted neurosurgery. The addition of theendoscope provided excellent visualiza-tion of the anterolateral aspect of the

ndylar transtubercular approach (right side). (A)medulla, the endoscope is advanced below) The green arrow indicates the corridor gainedretracted dura laterally, the accessory nerveperiorly. (C) With a superior medial retraction ofwas advanced above CN X, just inferolateral tos, vertebrobasilar junction, proximal basilarlet of the abducens nerve is seen at the lowerin a slightly more cranial direction, we could

Meckel cave and the abducens nerve enteringrt of the cavernous sinus. The caudal loop ofcerebellar artery (SCA) projects toward and

ve is identified within the tentorial incisura justerve passes between the posterior cerebellar

ar foramen laterally and the facial andlateral end of the pontomedullary sulcus,The most superior part of the cerebellopontine anglering the internal acoustic canal and the relationshipry; A.I.C.A., anteroinferior cerebellar artery; Bas., basS.C.A., superior cerebellar artery; Vert., vertebral.

brainstem, CNs III through XII, the verte-

WORLD NEUROSURGE

bral arteries bilaterally, PICA, anteriorspinal artery, VB junction, and the basilarartery and its branches; in addition, theupper part of the cerebellopontine anglecould be observed (Figure 6). The endo-scope was introduced through threecorridors: superiorly above CN X and in-ferolateral to the flocculus, lateral to me-dial through the enlarged space createdby the removal of the JT between CN IXand CN XI, and inferomedial beneath CNIX to view the craniovertebral junction

the Meckel cave to the internal acoustic canal,the AICA is appreciated; also, the trigeminalhor., choroid; C.N., cranial nerve; P.C.A., posterior

pracoto theion. (B

by theves sucopearteriee rootwardof theior paperiorar nerotor njugul

at thes. (G) e, fromes ent with., arte ilar; C

(Figure 6).

RY, DOI:10.1016/j.wneu.2011.03.024

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PEER-REVIEW REPORTS

VITTORIO M. RUSSO ET AL. MIST APPROACH TO THE LOWER CLIVUS

Clinical Application of the ApproachThe MIST approach requires a detailed un-derstanding of the complex anatomy of thecondylar fossa, hypoglossal canal, emissaryveins, JT, and jugular bulb (Figures 1 and 3)(6, 20). Before attempting the approach, adetailed preoperative workup, includingmagnetic resonance imaging, magneticresonance angiography, and computed to-mographic reconstructions, should be per-

Figure 7. (A) Superior view of the skull base. In tjugular tubercle is drilled out in a superoanteromplane. The red arrow indicates the direction of tguidance snapshot of a cadaveric specimen. Theand access to the premedullary cistern. For., for

Table 1. Anatomic Structures Exposedin Front of and Lateral to the InferiorBrainstem by the MIST and theExtended FL Approaches

MIST FLSC/FLTC

VA4 10/10 10/10

PICA orig. 10/10 10/10

PICA 10/10 10/10

VBJ 10/10 10/10

ASpA 1/10 10/10

CN IX-XI 10/10 10/10

CN XII 10/10 10/10

Prox. SpN XI 0/10 10/10

Prox. Dent. Lig. 0/10 10/10

ASpA, anterior spinal artery; CN, cranial nerve; Dent.,dentate; FLST, far lateral supracondylar transtuber-cular; FLTC, far-lateral transcondylar; Lig., ligament;MIST, minimally invasive supracondylar transtuber-cular; Orig., origin; PICA, posteroinferior cerebellarartery; Prox., proximal; SpN, spinal nerve; VA4, fourthsegment (intradural) of the vertebral artery; VBJ,vertebrobasilar junction.

formed in order to visualize the detailed F

WORLD NEUROSURGERY 77 [5/6]: 704-7

natomy of the osseous and neurovasculartructures.

Extradural resection of the JT is chal-enging. The maneuver is performedhrough a narrow corridor with limitedisualization. Aberrant or enlarged jugu-ar bulb anatomy can limit access to theupracondylar fossa, preventing extra-ural JT resection. The use of intraopera-

ive image guidance is strongly recom-ended in order to visualize the important

natomic relationships and to maintainhe correct angle of drilling and define theepth of JT resection (Figure 7).

Potential applications of the MIST ap-roach include discrete neoplastic le-ions located at the pontomedullary junc-ion. The approach can also be applied toascular lesions of the VB junction andelective PICA–VA aneurysms. When theICA take-off is located rostral to the hy-oglossal canal, adequate exposure isossible through a MIST approach. How-ver, when more proximal VA control isequired or when the PICA origin is cau-al to the hypoglossal canal, removal of

he occipital condyle and likely the C1rch will be required (19, 32).

Primary or adjunctive endoscopic neu-osurgical approaches have gained widecceptance in neurosurgical practice (8,, 16, 17, 23, 30). Future applications ofeuroendoscopy will likely reflect less-in-asive alternatives of traditional skullase approaches. We evaluated the MISTombined with endoscopy as a potentiallternative to the traditional extended

pracondylar transtubercular approach, thedirection, approximately 45 degrees in the axialgical view after the tuberculectomy. (B) Imagelar tubercle (red star) blocks the surgical view; Jug., jugular; Occip., occipital; Tub., tubercle.

LA. Three distinct endoscopic working

12, MAY/JUNE 2012 ww

orridors were identified that, when com-ined with the microsurgical exposureained through the MIST, provided nearly

dentical exposure compared to the ex-ended far-lateral microscope-only ap-roach. Extensive experience with basicndoscopic techniques, including intro-uction between neurovascular struc-

ures and working with two-dimensionalisualization, is strongly recommendedefore applying these techniques to theIST or any other minimally invasive op-

rative corridors.

ONCLUSION

he MIST procedure is a minimally invasivelternative to the extended far-lateral whenpproaching selective pathology of the lat-ral medulla and lower clivus. Furthermore,he adjunctive use of the endoscope pro-ides enhanced visualization of the vascu-ar, neural, and bony structures, with mini-

al retraction of the cerebellum and cranialerves. The MIST has the potential to mini-ize morbidity associated with the tradi-

ional far-lateral approach.

CKNOWLEDGMENT

ittorio M. Russo, Francesca Graziano, andonica Quiroga have contributed equally to

he work.

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WORLD NEUROSURGE

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onflict of interest statement: The authors declare that therticle content was composed in the absence of anyommercial or financial relationships that could beonstrued as a potential conflict of interest.

eceived 10 September 2010; accepted 22 March 2011

itation: World Neurosurg. (2012) 77, 5/6:704-712.OI: 10.1016/j.wneu.2011.03.024

ournal homepage: www.WORLDNEUROSURGERY.org

vailable online: www.sciencedirect.com

878-8750/$ - see front matter © 2012 Elsevier Inc.

6. King WA, Wackym PA, Sen C, Meyer GA, Shiau J,Deutsch H: Adjunctive use of endoscopy during pos-

lar artery to cranial nerves VII-XII. Clin Anat 20:886-891, 2007. All rights reserved.

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