ANATOMIC REPORT

ENDOSCOPIC TRANSORAL-TRANSCLIVAL APPROACH TO

THE BRAINSTEM AND SURROUNDING CISTERNAL SPACE:ANATOMIC STUDY

Oreste de Divitiis, M.D.Neurosurgical Clinic, University ofMessina School of Medicine,Messina, Italy

Alfredo Conti, M.D.Neurosurgical Clinic, University ofMessina School of Medicine,Messina, Italy

Filippo Flavio Angileri,M.D.Neurosurgical Clinic, University ofMessina School of Medicine,Messina, Italy

Salvatore Cardali, M.D.Neurosurgical Clinic, University ofMessina School of Medicine,Messina, Italy

Domenico La Torre, M.D.Neurosurgical Clinic, University ofMessina School of Medicine,Messina, Italy

Manfred Tschabitscher,M.D.Microsurgical and EndoscopicAnatomy, University of Vienna,Vienna, Austria

Reprint requests:Oreste de Divitiis, M.D.,Neurosurgical Clinic, University ofMessina, Policlinico Universitario,Via Consolare Valeria 1, 98125,Messina, Italy.Email: odedivitiis@unime.it

Received, January 27, 2003.

Accepted, August 27, 2003.

OBJECTIVE: The purpose of this study was to review the endoscopic anatomic featuresof the anterior brainstem and surrounding cisternal spaces via a transoral-transclivalapproach.METHODS: Fifteen adult human cadaveric heads, obtained from 10 fresh cadaversand 5 formalin-fixed cadavers, were used to demonstrate both the feasibility of anendoscopic transoral-transclival intradural approach and its exposure potential. Toanalyze the exact extension of a safe entry zone through the clivus, 20 skull bases wereused to obtain anatomic measurements.RESULTS: The transoral approach was performed without maxillotomy or mandibu-lotomy and with a clival opening of 20 by 15 mm. Such a limited clival and duralopening allowed the insertion of the endoscope and instruments, full visualization ofthe anterolateral brainstem and cisternal spaces around it, and reconstruction of allanatomic layers by means of a paraendoscopic technique.CONCLUSION: The endoscopic transoral-transclival approach enables full access tothe anterolateral brainstem and to the cisternal space around it. The use of theendoscope has the potential to reduce the need for a wider cranial base opening andthe danger of postoperative complications.

KEY WORDS: Anatomy, Brainstem, Neuroendoscopy, Transoral-transclival approach

Neurosurgery 54:125-130, 2004 DOI: 10.1227/01.NEU.0000097271.55741.60 www.neurosurgery-online.com

The anterior brainstem and the vertebro-basilar junction are involved in a num-ber of neurosurgical disorders, such as

extra-axial and intrinsic tumors, aneurysms,and vascular malformations. Nevertheless,they have long been considered a “no-man’sland” (15). The development of the modernconcept of cranial base surgery has providedthe neurosurgeon with the technical and ana-tomic awareness to deal with these challeng-ing anatomic structures. A number of differ-ent approaches to these regions have beendeveloped through anterior, anterolateral, andposterolateral routes (11, 16, 17, 30, 31, 33–39).Nevertheless, these cranial base surgical ap-proaches are, in some instances, highly de-structive; others require a high degree of ce-rebral and vascular manipulation, in contrastwith the modern concept of keyhole surgery.

Anatomically, the most physiological andshortest route to the anterior surface of thebrainstem is represented by an approach per-

formed through the pharynx and the under-lying clival bone. This approach offers a directview of the anterior brainstem and vertebro-basilar junction without requiring dislocationor manipulation of any cerebral or vascularstructure. The transoral approach is consid-ered effective for giving access to ventrallylocated abnormalities of the clivus and cranio-vertebral junction, and it has been used exten-sively for treatment of extradural lesions (2, 7,12, 19, 21, 25).

A transoral-transclival approach to the in-tradural compartment was described for thefirst time by Mullan et al. (26) in 1966 for thetreatment of an extra-axial tumor. Since then,the approach has been used to treat mainlymidbasilar or vertebrobasilar junction aneu-rysms (13, 27, 32, 41). In 1991, Crockard andSen (6) reported seven intradural lesions op-erated on via this approach; the lesions com-prised meningiomas and neurofibromas.More recently, Perneczky’s group reported

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two cavernous angiomas of the brainstem treated by thisapproach (28). Aside from these studies, few series and alimited number of cases (29) have been reported, probablybecause of the technical difficulties (such as the need forworking in a narrow and deep cavity and the lack of properinstrumentation) or because of the likelihood of postoperativecomplications, such as cerebrospinal fluid leakage or velopha-ryngeal incompetence (6, 13, 18, 20, 27, 32, 38, 40).

Endoscopy has technical characteristics that offer the poten-tial to overcome such difficulties (3, 4, 8, 15). The aims of thisstudy were to demonstrate the feasibility of this approach andits exposure potential through a limited clival and dural open-ing and to describe the anatomic features of an intraduraltransoral-transclival approach from the endoscopicperspective.

MATERIALS AND METHODS

This anatomic study was performed at the Institute of Anat-omy of the University of Vienna, Austria. Fifteen cadaverheads were used for the study, 10 from fresh cadavers and 5from formalin-fixed cadavers. The arteries of 10 fresh speci-mens and both the arteries and veins of 5 formalin-fixedcadavers were injected under pressure with colored siliconerubber (Dow Corning, Midland, MI) via internal carotid arter-ies and internal jugular veins. The endoscopes used were rigid0-, 30-, 45-, and 70-degree rod lens endoscopes 2.7 or 4 mm indiameter and 11 or 18 cm in length (Karl Storz, GmbH & Co.,Tuttlingen, Germany).

The specimens were placed in a slightly extended positionin a four-point pin headrest. A self-retaining retractor systemwas positioned to keep the mouth open. The soft palate wassplit in the midline and fixed with sutures. The hard palatewas left in place. The pharyngeal mucosa was incised from theanterior arch of the atlas upward through the vault of thenasopharynx to the posterior border of the vomer. The muco-periosteal layer was retracted laterally, exposing the clivusand the craniovertebral junction. On the clival surface, thepharyngeal tubercle was identified, and a clival craniectomywith an average diameter of 20 mm in length and 15 mm inwidth was initiated just above it with a high-speed drill. Thedura mater was visualized and opened with a vertical incision.A video recorder (S-VHS SVO 9500 MDP; Sony, Tokyo, Japan)and a video-capture system (Digital Still Recorder; Sony) wereused for digital acquisition of the endoscopic pictures.

To analyze the exact extension of a safe entry zone throughthe clivus, we obtained anatomic measurements in 20 skullbases. We measured the length of the retropharyngeal surfaceof the clivus, and we measured its width at three points: at thebase between the occipital condyles, at the level of the pha-ryngeal tubercle, and at the upper portion of the border withthe vomer. The distances between hypoglossal channels, jug-ular foramina, and inferior petrous sinuses were also mea-sured. Finally, the distance of the clivus from the superioralveolar arch was measured to evaluate the depth of thesurgical field.

RESULTS

Bone Measurements

Figure 1, A and B, shows the distances that were measuredbetween the anatomic structures that may be jeopardizedduring the transclival approach. Table 1 summarizes thesemeasurements and those obtained by measuring the depth ofthe surgical field and the extension of the exposed clivalsurface.

Endoscopic Procedure

After opening the dura mater, the premedullary, the pre-pontine, and the lateral cerebellomedullary cisterns came intodirect view (Fig. 2, A and B). The vertebral arteries could be

FIGURE 1. Intraoperative views of the extracranial (A) and intracranial(B) surfaces of the clivus. The overall length of the retropharyngeal surfaceof the clivus from the vomer to the foramen magnum (h) and its width atthree points—at the border with the vomer (D1), at the level of the pha-ryngeal tubercle (D2), and at the base between the occipital condyles(D3)—were measured. The distances between the inferior petrous sinuses(D4), the jugular foramina (D5), and the hypoglossal channels (D6) werealso measured on the intracranial surface to analyze a zone of safe entrythrough the clivus.

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followed along their cisternal course up to the vertebrobasilarjunction at the pontomedullary junction. The origin of the twoposteroinferior cerebellar arteries and the anterior spinal ar-tery, as they originated from the vertebral arteries, were visi-ble in the anteriormost lateral cerebellomedullary cistern andin the premedullary cistern, respectively. The fibers originat-ing in Cranial Nerve XII in the preolivary sulcus were alsoobserved at this level. In the prepontine cistern, the basilarartery could be visualized in the lower two-thirds of the field,permitting observation of the typical variability of dimensionand course (31). The abducens nerve was identified and fol-lowed along its course in this cistern toward Dorello’s canal.

By means of a 30- to 45-degree optic lens and a lateralinclination of the endoscope, it was possible to reach thecerebellopontine cistern from a premeatal route. Along thecourse of the anteroinferior cerebellar artery, the acoustic-facial bundle was identified and followed along its free cister-nal course to the internal acoustic channel (Fig. 3, A and B).Anatomic features of the internal acoustic channel could beobserved as a result of the optic properties of the endoscope(Fig. 3B). At this level, it was also possible to visualize thelabyrinthine arteries in their course toward the internal acous-tic channel (Fig. 3, B and C).

Turning the endoscope rostrally and using the same angledoptic lens at 30 degrees and 45 degrees, the upper part of thecerebellopontine angle was explored. The main structure un-der this view was represented by the trigeminal nerve alongits course from the pons toward Meckel’s cave (Fig. 3D). Byusing the same angled optic lens and turning the endoscopelaterally and downward, it was possible to reach the posteriorpart of the lateral cerebellomedullary cistern (Fig. 3, A and C).The interpeduncular fossa was also reached with this ap-proach. Angled optic lenses at 45 or 70 degrees were needed toachieve good visualization. The endoscope was directed up-

ward with an inclination of approximately 45 degrees, follow-ing the basilar artery to its superior third, which was hiddenby the border of the clival craniectomy. It was thus possible toreach and thoroughly explore the interpeduncular cistern (Fig.4A).

The perforating branches of the basilar tip and of P1 werevisible in detail and could be followed to their entrance in theposterior perforated substance (Fig. 4B). The posterior com-municating arteries appeared in the anterolateral part of thesurgical field, where they crossed Liliequist’s membrane toreach the posterior cerebral arteries with a lateral deflection(Fig. 4C). The mammillary bodies and the tuber cinereum werealso visualized (Fig. 4D). The identification of the oculomotornerves completed the exploration of the cistern (Fig. 4, A–C).

DISCUSSION

Minimizing surgical trauma means fewer complications,shorter hospital stays, and reduced overall psychological con-sequences. Endoscopy is a leading technique of minimallyinvasive neurosurgical procedures. Recently, an important im-

FIGURE 2. By use of 0-degree optics, the premedullary (A) and prepon-tine cisterns (B) were visualized. The lower basilar artery (BA) and thevertebrobasilar junction were in direct view after the dura mater wasopened. The anterior spinal artery (ASA) descending from the two verte-bral arteries (VA) was visible at the pyramid decussation and could be fol-lowed down to the spinomedullary junction. The origin of the posteroinfe-rior cerebellar artery (PICA) could also be identified at this level. Theorigin of the anteroinferior cerebellar artery (AICA) and the perforatingbranches could be visualized along the course of the basilar sulcus to theupper part of the basilar artery, at the border of the interpeduncular cis-tern. In the prepontine cistern, the entire free course of both abducensnerves (VI) could be followed from their origin in the pontomedullary sul-cus to Dorello’s canal.

TABLE 1. Data obtained measuring the mutual distances ofstructures surrounding the clival opening, the depth of thesurgical field, and the length of the exposed clival surface

Measurement Distance (mm)

Length of the exposed clival surface 29 (24–38)

Depth of the surgical field 20 (16–27)

Distance between occipital condyles 20 (16–27)

Distance between petroclival sutures (atthe level of the pharyngeal tubercle)

27 (18–35)

Distance between petroclival sutures (atthe level of the vomer)

21 (17–26)

Distance between hypoglossal channels 41 (36–44)

Distance between jugular foramina 60 (49–65)

Distance between inferior petrosal sinuses 21 (18–25)

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pulse in the development of endoscopic surgery was providedby the introduction of the transnasal-transsphenoidal ap-proach for surgery of the sellar and parasellar regions (3, 9, 10,23). This experience has spurred the search for new surgicalapproaches that would enable access to the entire cranial baseby the use of minimally invasive techniques (1, 22–24).

The use of the endoscope offers several theoretical advan-tages when dealing with the transoral-transclival approach. Inour anatomic study, we demonstrated that this approach en-ables full access to the anterolateral brainstem and to thecisternal space around it, from the spinomedullary junction tothe interpeduncular cistern, including a thorough vision of thevertebrobasilar arterial system and of Cranial Nerves III to XII.This endoscopic approach thus provides excellent visualiza-tion of some of the most challenging and inaccessible territo-

ries of the brain, without requiring extended cranial basedestruction.

Furthermore, most of the limitations of the transoral-transclival procedure may potentially be reduced by the use ofan endoscopic approach. Crockard and Sen (6) suggested aclival opening of 2 by 3 cm for dealing with intradural lesions;in this study, the opening was limited to 20 mm in length and15 mm in width. Such an opening was demonstrated to besufficient for the endoscopic view, and it was located in a “safeentry zone” through the clivus, which we tried to delineate byobtaining the bone measurements. These data, although al-ready in the literature, were revised in this light to define thelimits of the clivectomy.

It is also worth noting that both labiomandibuloglossotomyand maxillotomy, which are often required with microscopicprocedures to increase the view caudally and rostrally, werenot needed, and the reduced opening through the clivus didnot limit the complete exploration of the cisternal spaces. Alimited clival opening can reduce the risk of injuring thecondyles with subsequent postoperative instability. Another

FIGURE 3. By use of a 30- to 45-degree optic lens and a lateral inclina-tion of the endoscope, it was possible to enter the cerebellopontine cisternvia a premeatal route. Along the anteroinferior cerebellar artery (AICA)course, the acoustic-facial bundle (VII–VIII) was identified and followedalong its free cisternal course to the internal acoustic channel (IAC).Because of the optic properties of the endoscope, it was possible to followthe nerves to their entrance into the IAC and to observe their anatomicfeatures. The VII–VIII bundle was encircled by the loop formed by theAICA. At this level, it was possible to visualize the labyrinthine arteries(LbA) in their course toward the IAC (B and C). By using the sameangled optic lens, and by turning the endoscope laterally and downward,it was possible to reach the posterior part of the lateral cerebellomedullarycistern. It was possible to identify the IX and X nerves (IX–X) runninglaterally and posteriorly from the retro-olivar sulcus to the jugular fora-men, covered in their anterior portion by a tuft of the choroidal plexus(CP) exiting from the foramen of Luschka and by the variable looping ofthe posteroinferior cerebellar artery (A and C). By turning the endoscoperostrally and using the same angled optic at 30 and 45 degrees, it waspossible to explore the upper part of the cerebellopontine angle. The mainstructure under this view was represented by the trigeminal nerve (V). Itwas observed along its course from the pons directed anteriorly and supe-riorly toward Meckel’s cave (D).

FIGURE 4. The interpeduncular cistern was reached by using a 70-degreeoptic and an upward inclination of the instrument, following the basilarartery (BA) to its superior third. In this cisternal space, the visual fieldwas limited by the tuber cinereum superiorly, Liliequist’s membraneanterolaterally, and the optic tracts posterolaterally. The basilar tip, thebasilar bifurcation, the superior cerebellar arteries (SCA), and the P1tracts of the posterior cerebral arteries were completely visible. The perfo-rating branches of the basilar tip and of P1 were visible in detail and werefollowed to their entrance into the posterior perforated substance. The pos-terior communicating arteries (PcoA) appeared in the anterolateral part ofthe surgical field, where they crossed Liliequist’s membrane with a lateraldeflection to reach the PCA. Above the posterior perforated substance andposteriorly to the tuber cinereum, mammillary bodies (MB) were also visu-alized. The identification of the oculomotor nerves (III) completed theexploration of the cistern. They coursed from the interpeduncular fossa,passing between the SCA and PCA in an anterior and superior directiontoward the tentorial edge.

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potential advantage is represented by the preservation of bet-ter velopharyngeal function. A wide clival defect is responsi-ble for the incompetence between the posterior pharyngealwall and the soft palate, resulting in difficulties in swallowingand in phonation.

The dural opening was minimized; it was sized to allow theintroduction of the endoscope and the instruments. With thisapproach, it was possible to suture the dura, even though it wasmuch deeper than the atlantic arch. This suturing was accom-plished by using a paraendoscopic technique, which allowedfirm packing and safe sealing (Fig. 5). Both the limited clival anddural opening, with the possibility of reconstructing each ana-tomic layer, may represent the basis for a reduced occurrence ofpostoperative cerebrospinal leakage and infection, which repre-sent the main complications of the standard approach.

A minimally invasive approach should be well grounded onanatomic investigations. This study provides a description ofanatomic structures that, although widely known by neuro-surgeons, are presented from a new perspective, as a result ofeither the different pathway used or the different optical in-struments. The view of the anterior aspect of the brainstemoffered in this study may appear, as often happens in ana-tomic dissection studies, to be simply an idealistic construc-tion. However, it is worth noting that the surgical procedurewas similar to that used in the standard microscopic approachand that the exposure widening was attributable to the possi-bility of reaching blind angles.

The application of this approach is, at present, still far fromclinical practice. However, clinical findings on the use of anendoscopic transoral-transpharyngeal approach to treat

craniocervical junction abnormalities have been reported, andthe endoscope was also used to assist in the removal of twobrainstem cavernous angiomas and a clival ecchordosis phys-aliphora (5, 14, 28). New technologies and instrumentation,such as instruments able to work through deep keyholes andwith angled tips to reach blind angles, new clip applicators, orcatheter ultrasound, will make surgical practice easier. Thestrategy for the endoscopic transoral-transclival approach willpresumably be selective and aimed mainly at lesions of thelower ventral brainstem, such as aneurysms, cavernous angi-omas, and small intra- and extra-axial tumors.

CONCLUSION

This study shows that the transoral-transclival route en-ables exploration of the cisterns surrounding the anterolateralbrainstem from the medulla to the lower diencephalon bymeans of the endoscope. We obtained a new and originalvisual perspective of these anatomic structures. The use ofminimally invasive endoscopic techniques has the potential toreduce the need for a wider cranial base opening and todecrease the danger of postoperative complications.

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COMMENTS

de Divitiis et al. have provided an anatomic rationale for anendoscopic transoral-transclival approach to the brain-

stem. They have arguably demonstrated that the technique isfeasible and that it provides adequate access to the ventralbrainstem. Their anatomic and descriptive portrayal is com-pelling. Clinical follow-up will determine whether this ana-tomic study will lead to improved patient outcomes andsafety. The authors’ efforts are significant and meticulous.

Edward C. BenzelCleveland, Ohio

The authors have completed a basic theoretical study of theadjunctive use of the endoscope in a transoral-transclival ap-

proach to the intradural structures. The study demonstrates thataccess can be expanded through this approach with the use of theendoscope. Although various clinical factors may result in this ap-proach not gaining wide acceptance or common clinical use, this isa useful article in guiding such attempts. I would also comment thatusing such anatomic studies as one’s own platform for clinicalapplication of the endoscope is insufficient. Rehearsal in the labora-tory on one’s own, developing the necessary facility with the endo-scope, and working with the altered view provided are also com-ponents of a necessary first step. The authors make a case for theincreasing usefulness of the endoscope as an adjunctive imagingtool in neurosurgery.

John Diaz DayPittsburgh, Pennsylvania

In this article, de Divitiis et al. have performed a study of anendoscopic transclival approach to the clivus and the brainstem. It

is clear that the endoscope allows more structures to be visualizedthan the microscope (1, 2). However, an important question iswhether the surgeon can “not only look, but actually do” (i.e.,operate) with the endoscope; for instance, if there were to be bleed-ing from a branch of the basilar artery, can the surgeon stop thebleeding and repair the artery? If a cranial nerve is damaged, can itbe repaired? An additional problem with an intradural transoral-transclival approach is repair of the dura at the end of the procedureto prevent meningitis. This is a significant problem with both theendoscope and the microscope. We need to make more progresswith regard to techniques than an anatomic study like this allowsbefore we can start using this technique with confidence.

Laligam N. SekharGreat Neck, New YorkDinko StimacAnnandale, Virginia

1. Kalavakonda C, Sekhar LN, Ramachandran P, Hechl P: Endoscope-assistedmicrosurgery for intracranial aneurysms. Neurosurgery 51:1119–1127, 2002.

2. Puxeddu R, Lui MW, Chandrasekar K, Nicolai P, Sekhar LN: Endoscopic-assisted transcolumellar approach to the clivus: An anatomical study. Laryn-goscope 112:1072–1078, 2002.

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