Abstract
Introduction The clival, paraclival, and craniocervical junction regions are challenging surgical targets. To approach these areas, endoscopic endonasal transclival approaches (EETCAs) and their extensions (far-medial approach and odontoidectomy) have gained popularity as they obviate manipulating and working between neurovascular structures. Although several cadaveric studies have further refined these contemporary approaches, few provide a detailed step-by-step description. Thus, we aim to didactically describe the steps of the EETCAs and their extensions for trainees.
Methods Six formalin-fixed cadaveric head specimens were dissected. All specimens were latex-injected using a six-vessel technique. Endoscopic endonasal middle and inferior clivectomies, far-medial approaches, and odontoidectomy were performed.
Results Using angled endoscopes and surgical instruments, an endoscopic endonasal midclivectomy and partial inferior clivectomy were performed without nasopharyngeal tissue disruption. To complete the inferior clivectomy, far-medial approach, and partially remove the anterior arch of C1 and odontoid process, anteroinferior transposition of the Eustachian–nasopharynx complex was required by transecting pterygosphenoidal fissure tissue, but incision in the nasopharynx was not necessary. Full exposure of the craniocervical junction necessitated bilateral sharp incision and additional inferior mobilization of the posterior nasopharynx. Unobstructed access to neurovascular anatomy of the ventral posterior fossa and craniocervical junction was provided.
Conclusion EETCAs are a powerful tool for the skull-base surgeon as they offer a direct corridor to the ventral posterior fossa and craniocervical junction unobstructed by eloquent neurovasculature. To facilitate easier understanding of the EETCAs and their extensions for trainees, we described the anatomy and surgical nuances in a didactic and step-by-step fashion.
Keywords: skull base surgery, middle and inferior clivectomies, odontoidectomy, far-medial approach, foramen lacerum, pterygosphenoidal fissure
Introduction
Surgically treating lesions of the clivus and surrounding structures is challenging. 1 2 3 While numerous approaches and trajectories have been effectively utilized, including retrosigmoid, transpetrosal, and anterior craniofacial, they may require extensive brain retraction and manipulation or extensive destruction of craniofacial structures and may not be ideal for certain pathologies. 1 4 5 6 Despite these extensive approaches, the surgeon is often operating between small windows by eloquent neurovascular structures. 7 8 9
To reach the clivus, ventral jugular foramen, occipital condyle, and craniocervical junction, endoscopic endonasal transclival approaches (EETCAs) and their extensions have gained popularity as they provide excellent illumination and magnification, and a surgical trajectory ventral to the neurovasculature of the cerebellopontine angle. 1 8 9 10 11 12
Although publications describing the EETCAs and their extensions are available, they often provide a general anatomical overview without didactic descriptions and illustrations of the steps involved in their execution. 1 8 9 10 13 14 15 16 Consequently, the main goal of this study is to develop an educational resource to help trainees understand the pertinent anatomy and procedural steps involved in safely and effectively performing the EETCAs and their extensions.
Methods
All aspects of this study were approved by our Institutional Review Board and Biospecimens Committee, as required by standard protocols (17-005898).
Six cadaveric head specimens were dissected at the surgical anatomy laboratory at our institution. All specimens were formalin-fixed and latex-injected using a six-vessel technique.
A 0-degree and 30-degree endoscope (4 mm, 18 cm, Hopkins II, Karl Storz, Tüttlingen, Germany), attached to a high-definition camera and a digital video recorder system, was used together with a complete set of instruments for endoscopic endonasal skull base surgery. Following our dissections, the specimens were three-dimensional photo-documented with endoscopic techniques as previously described by our team. 17
Endoscopic endonasal middle and inferior clivectomies, bilateral far-medial approaches, and odontoidectomy were modularly performed. Dissections were performed by one dissecting author (E.A.). Supervision was provided by the senior authors (M.P.C. and C.D.P.-N.) and a PhD in skull-base anatomy with advanced neuroanatomy experience (L.C.P.C.L.). Each dissection was carried forward or repeated until the expected quality level was achieved so that each critical step was clearly documented.
Following successful dissection, representative cases were reviewed to emphasize basic principles of approach selection and planning.
Results
Patient Positioning and Nasal Cavity Inspection
The specimens were placed in the simulated supine position in reverse Trendelenburg to approximately 15°. Subsequently, endoscopic inspection of the nasal cavities began.
Nasoseptal Flap Harvesting
The right middle and superior turbinates were gently lateralized and the dissection proceeded along the middle and superior nasal corridors. The ostium of the sphenoid sinus was identified medial to the superior turbinate, 1.5 cm above the superolateral angle of the posterior choana ( Fig. 1A ).
To harvest the nasoseptal flap, the superior incision started at the sphenoid ostium and ran parallel to the skull base approximately 1 cm inferior to the olfactory sulcus. When the incision reached the level of the anterior attachment of the middle turbinate, it was directed superiorly to incorporate the most anterosuperior area of the septal mucosa ( Fig. 1B ). The inferior incision started at the superior margin of the choana and extended inferomedially to meet the nasal cavity floor ( Fig. 1C ). The inferior incision continued anteriorly along the junction of the septum and nasal floor to the anterior margin of the septum. The incision progressed anteriorly along the nasal vault to the anterior edge of the septum ( Fig. 1D ). Finally, the superior and inferior incisions were connected with a vertical incision at the mucocutaneous junction. The nasoseptal flap was elevated from the septal cartilage and bone in a subperichondrial/subperiosteal plane ( Fig. 1E ). Preservation of the vascular pedicle was confirmed and the flap was stored in the nasopharynx ( Fig. 1F ). 18
Endoscopic Endonasal Bilateral Complete Ethmoidectomy, Right Medial Maxillectomy, and Transethmoidal Sphenoidotomy
Bilateral anterior and posterior ethmoidectomies, transethmoidal sphenoidotomies, and right type A medial maxillectomy were modularly performed. After the right type A medial maxillectomy was completed, the nasoseptal flap was stored from the nasopharynx to the right maxillary sinus.
The intra-sphenoidal septations were drilled flush with the floor of the sella, and the bony landmarks of the posterior wall of the sphenoid sinus were identified. These included the optic prominences, prechiasmatic sulcus, tuberculum recess, sellar prominence, clival recess, carotid prominences, and lateral optic-carotid recesses ( Fig. 2A ).
Endoscopic Endonasal Midclivectomy and Partial Inferior Clivectomy with Nasopharyngeal Preservation
The rostrum sphenoidale was fractured and removed. Bilaterally, the inferior and medial portions of the vidian canals were progressively drilled out and followed posteriorly to identify the anterior limit of the foramen lacerum at the most posterior portion of the vidian canal ( Fig. 2B ). Subsequently, the floor of the sphenoid sinus and the vaginal process of the sphenoid bone were drilled, exposing the medial aspect of the pterygosphenoidal fissure (i.e., synchondrosis between the lacerum process of the medial pterygoid plate and the floor of the sphenoid bone). 19 The lacerum process of the medial pterygoid plate, located inferomedial to the vidian canal, was drilled, identifying the lateral aspect of the pterygosphenoidal fissure and exposing the medial limit of the foramen lacerum. The fibrous tissue of the pterygosphenoidal fissure provides an excellent surgical landmark that can be followed during the endoscopic endonasal approach to foramen lacerum. 19 20 21 22 The vidian nerve was followed posteriorly within its canal until the lower portion of foramen lacerum was identified. 19 21 23 24 The pterygoid tubercle (i.e., triangular-shaped bony prominence located on the posterior surface of the medial pterygoid plate, medial to the vidian canal) was identified at the posterior convergence point between the pterygosphenoidal fissure and vidian canal. 19 21 The pterygoid tubercle was drilled, exposing the anterior limit of the foramen lacerum ( Fig. 2C ).
The internal carotid artery (ICA) was skeletonized starting from the dura of the anterior wall of the cavernous sinus to its lacerum segment, thus maximizing mobilization of the paraclival ICA and providing access to the medial petrous apex located just posteriorly ( Fig. 2D ). 19 After the paraclival ICAs were skeletonized bilaterally, the clival bone located immediately posterior and medial to the pterygosphenoidal fissure was removed laterally up to the petroclival fissure, exposing the ICA as it emerges from the carotid canal ( Fig. 2E ).
Clival drilling proceeded inferiorly until visualization was obstructed by the floor of the sphenoid sinus. This exposure afforded better access to the medial petrous apex located just posterior to the paraclival ICA. To expose medial aspect of the lacerum ICA, clival bone immediately posterior and medial to the pterygosphenoidal fissure was completely removed. Just medial to the paraclival ICAs bilaterally, the abducens nerve was identified at the level of its proximal (and inferomedial) portion. While maintaining the integrity of the pharyngobasilar fascia with the muscles of the posterior nasopharynx, the superior portion of the lower clivus could be removed using a 70° angle drill and a 45° endoscope angled inferiorly ( Fig. 2F ).
A linear, midline dural incision was made, and the anterior pontine membrane and underlying neurovascular structures within the prepontine cistern came into view ( Fig. 2G ). The anterior prepontine membrane was removed, and the ventral brainstem and associated neurovascular structures were identified. Specifically, structures visualized included the upper third of the medulla, the ventral pons, the intradural segment of the vertebral arteries, basilar artery, pontine arteries, anterior inferior and posterior inferior cerebellar arteries, cisternal segments of the abducens nerves, and transverse pontine vein ( Fig. 2H–N ). 25
Endoscopic Endonasal Complete Inferior Clivectomy and Partial-Superior Removal of the Anterior Arch of C1, and Partial-Superior Odontoidectomy (with Bilateral Incision of the Pterygosphenoidal Fissure Tissue and Anteroinferior Transposition of the Eustachian–Nasopharyngeal Complex)
The anatomy around the inferior portion of the foramen lacerum was better explored in order to identify relevant surgical landmarks. The foramen lacerum is filled in its inferior portion with fibrocartilaginous tissue that is strictly connected to the pharyngobasilar fascia inferomedially, the pterygosphenoidal fissure anteriorly, the petroclival fissure posteroinferiorly, and the petrosphenoidal fissure posterolaterally. 19 20 21 23 The Eustachian tube, traditionally divided into a proximal osseous and a distal cartilaginous portion, can be divided into five segments in an anterior-to-posterior direction accordingly to an endoscopic endonasal surgically oriented classification, including the nasopharyngeal, pterygoid, lacerum, petrous, and bone segments. 19 20 21 23 The lacerum segment of the Eustachian tube runs just inferior to and attaches to the fibrocartilaginous portion of the foramen lacerum. 19 Then the Eustachian tube passes the scaphoid fossa (pterygoid segment), and continues anteromedially and inferiorly to the posterolateral wall of nasopharyngeal cavity (nasopharyngeal segment). 19 21
The junction between the fibrocartilaginous tissues of the inferior foramen lacerum and the cartilage of the lacerum segment of the Eustachian tube was transected. The pterygosphenoidal fissure serves as a safe entry zone to the inferior foramen lacerum region. This sublacerum corridor along the inferior aspect of the petrous apex provides a safe surgical trajectory toward the ventral aspect of the petroclival fissure and jugular foramen, while mitigating the risk of carotid artery injury. 19 22
The fibrocartilaginous tissues of foramen lacerum are also connected with the petroclival synchondrosis posterolaterally and the pharyngobasilar fascia anteromedially. 19 The disconnection of the fibrocartilaginous tissues of foramen lacerum from these two adhesions allows inferior transposition of the Eustachian tube and posterior nasopharynx ( Fig. 3A ). 26
The pharyngobasilar fascia and mucosa above torus tubarius were separated from the sphenoid sinus floor and medial pterygoid plate until the insertion of the pharyngobasilar fascia into the clival bone was reached ( Fig. 3B ). Further dissection detached the nasopharyngeal and pterygoid segments of the Eustachian tube. Once the fibrocartilaginous adhesions of the Eustachian tube, petroclival synchondrosis, and pharyngobasilar fascia were completely disconnected from the inferior portion of the foramen lacerum, the Eustachian–nasopharyngeal complex (i.e., Eustachian tube, prevertebral fascia, and longus capitis and rectus capitis muscles) was transposed inferiorly, better exposing the lower clivus and craniocervical junction ( Fig. 3C, D ).
The superior and inferior attachments of the anterior atlanto-occipital membrane were exposed and dissected from the bone, identifying the anterior arch of C1 and the bilateral atlanto-occipital joints ( Fig. 3E, F ). The inferior portion of the lower clivus and the superior portion of the anterior arch of C1 were drilled, exposing the tip of the odontoid process and apical ligament. The apical ligament was identified anterior to the alar and cruciate ligaments ( Fig. 3G ). By transecting the apical ligament and the bilateral alar ligaments, the superior crus of the cruciate ligament was identified and removed, providing visualization of the tectorial membrane ( Fig. 3H, I ). The superior portion of the odontoid process was then drilled ( Fig. 3J ). The superior attachment of the tectorial membrane was detached and transposed inferiorly, exposing the underlying clival and upper cervical dura. The dural incision was extended inferiorly, better exposing the proximal portion of the intradural vertebral arteries and the C1 nerve root.
Far-Medial Extension
Once the standard inferior clivectomy was completed, lateral extensions of the clivectomies were performed. To access the hypoglossal canal, the supracondylar groove was exposed deep to the atlanto-occipital joint capsule and was progressively drilled until exposure of the hypoglossal canal and its dural covering was afforded ( Fig. 3K, L ). To increase the lateral exposure towards the jugular foramen, the jugular tubercle was drilled laterally until the medial edge of the jugular foramen. This provided access to cranial nerves IX, X, and XI at their distal intracranial course ( Fig. 3M–P ).
Endoscopic Endonasal Complete Removal of the Anterior Arch of the Atlas and Odontoidectomy (with Bilateral Para-Eustachian Incision of the Posterior Wall of Nasopharynx)
The mucosal and muscular layers of the posterior nasopharynx and the pharyngobasilar fascia were incised just medial to the torus tubarius of the Eustachian tube bilaterally, and transposed inferiorly ( Fig. 4A ). Longus capitis, rectus capitis anterior, and anterior longitudinal ligament were exposed and inferiorly displaced to provide better access to the entirety of the anterior arch of C1, the atlantoaxial joint, and the anterior surface of the body of C2 ( Fig. 4B, C ). Bilateral osteotomies were performed at the lateral extents of the anterior arch of C1 and it was removed en-bloc ( Fig. 4D ). The base of the odontoid process was drilled and the odontoid process was removed, exposing the underlying cruciate ligament ( Fig. 4E ). The cruciate ligament and the tectorial membrane were incised and dissected exposing the upper cervical dura ( Fig. 4F, G ). The previous dural incision was extended inferiorly, better exposing the neurovascular anatomy of the upper cervical spinal cord, including the ventral C2 nerve root, spinal roots of the accessory nerve, and the distal portion of the extradural vertebral artery within sulcus arteriosus ( Fig. 4H ).
Representative Case Review
Case 1: Clival Chordoma Surgically Treated with Endoscopic Endonasal Midclivectomy and Partial-Inferior Clivectomy with Nasopharyngeal Preservation
A neurologically intact 31-year-old female with a history of headache underwent a brain magnetic resonance imaging (MRI) that revealed a clival lesion involving the middle and upper portion of the lower clivus, with intradural extension into the posterior cranial fossa. Mass effect on the ventral pons was present ( Fig. 5A, B ). An endoscopic endonasal midclivectomy and partial inferior clivectomy with nasopharyngeal preservation was utilized. Reconstruction was performed with collagen graft and right-sided nasoseptal flap. Gross total resection of the lesion was achieved ( Fig. 5C ). Histopathological examination confirmed the diagnosis of chordoma. The postoperative course was uneventful and the patient was discharged home on postoperative day 5. No adjuvant radiotherapy was given and the patient remains without evidence of disease 12 months after resection.
Case 2: Clival Chordoma Surgically Treated with Endoscopic Endonasal Midclivectomy and Partial-Inferior Clivectomy with Bilateral Para-Eustachian Nasopharyngeal Incision
A 52-year-old female with a history of episodes of blurred and double vision associated with headaches and nausea presented to our clinic for worsening symptoms. MRI showed a large intracranial clival lesion with bone erosion and intradural extension, involving the middle and lower clivus, sellar floor, and, bilaterally, the ventral jugular tubercle and occipital condyle ( Fig. 5D, E ). The patient initially underwent a C0–C2 fusion to prevent instability of the craniocervical junction (CCJ) followed 2 weeks later by an endonasal midclivectomy, partial inferior clivectomy, and bilateral far-medial extension, with para-Eustachian nasopharyngeal incisions for tumor resection. An aggressive subtotal resection was performed and reconstruction was performed with collagen graft and fat graft. The patient was neurologically stable after surgery. Histopathological examination confirmed the diagnosis of chordoma. She then received proton beam therapy to a total dose of 70 Gy and remains free from tumor progression 12 months following completion of therapy.
Case 3: Odontoid Process Fracture—Endoscopic Endonasal Odontoidectomy (with Bilateral Para-Eustachian Incision of the Posterior Wall of Nasopharynx)
A 53-year-old female with a history of Goldenhar syndrome presented to our clinic with worsening clumsiness in her right hand and sensory disturbances in all four extremities. MRI indicated posterior displacement of her C1–C2 vertebrae causing severe cervical stenosis and cranial settling. Given the progression of her symptoms, and multiple previous cervical surgeries, decompression of her CCJ was offered through an endoscopic endonasal inferior clivectomy and odontoidectomy. The patient was discharged home on POD 12 with no new neurological deficits.
Discussion
In this study we described the basic steps, anatomy, and nuances of the endoscopic endonasal middle and inferior clivectomies, far-medial approach, and odontoidectomy. We previously described the technique for anteroinferior transposition of the Eustachian–nasopharynx complex after transecting the soft tissues of the pterygosphenoidal fissure and disconnecting the fibrocartilaginous borders of the Eustachian tube with preservation of the nasopharyngeal mucosa. 19 22 Through the EETCAs, unobstructed access to neurovascular anatomy of the ventral brainstem was afforded.
Given the many neurovasculature structures that surround or are involved in the EETCAs, identification of landmarks that facilitate safe dissection is paramount. First, proper localization of foramen lacerum is crucial to minimize the risk of ICA injury. The vidian canal is the most useful landmark for the lacerum ICA from the endoscopic endonasal trajectory. 19 24 The vidian canal is located at the lateral aspect of the floor of the sphenoid sinus within the body of the pterygoid, and, once identified, can be carefully followed posteriorly to find the lacerum ICA as it turns vertically just medial to the vidian canal and its contents. The vidian canal converges posteriorly with the pterygosphenoidal fissure, and as drilling progresses in between them, the pterygoid tubercle will remain between the pterygosphenoidal fissure and the vidian canal to form the anterior inferior part of the foramen lacerum. 19
Several lesions of the posterior fossa may be amenable to EETCAs, including tumors, vascular malformations, and craniocervical junction abnormalities. 27 28 Benefits of the EETCA to lesions of the posterior fossa include a working corridor mostly medial to involved neurovasculature, adequate illumination and magnification of the operative field, and potentially early devascularization of the lesions' blood supply in case of meningiomas. 27 EETCAs are now commonly utilized for most chordomas of the clivus as the tumor's usually soft consistency facilitates its dissection away from involved neurovasculature. 5 8 29 30 31 32 33 34 35 36 37 38 39 40 41 42 Despite growing experience with these approaches, utilization of the EETCAs for other posterior fossa lesions—including meningiomas and vascular lesions—remains controversial. 43 44 For clival tumors, hesitancy in utilizing this approach may be the inability to perform bimanual dissection—especially when the lesion is suspected to be adherent to surrounding structures. For vascular lesions, difficulty in attaining control for aneurysms and controlling inadvertent bleeding for other malformations may obviate the use of the EETCAs. Despite these limitations, several publications have described this approach for petroclival/clival meningiomas, 43 44 aneurysms, 27 45 46 and cavernous malformations. 31 47 48 49 50 51 52 Approach selection for lesions that have anatomical equipoise should be guided by a surgeon's comfort with the different approaches. Endoscopic endonasal approaches have also been effective for treating craniocervical junction abnormalities. Indications for this approach have included severe basilar invagination, displaced os odontoideum, pannus with mass effect, and retroflexed odontoid processes associated with Chiari malformation Type 1. 27 53 With respect to open strategies for addressing these pathologies, however, the endoscopic endonasal approaches may be more invasive and offer more constrained corridors with limited surgical maneuverability.
Lateral extension of the corridor is often limited for most endoscopic endonasal approaches. For the EETCAs, lateral extension is limited by the paraclival ICA, Eustachian tube, and jugular foramen. 14 54 If a lesion extends lateral to these structures and an EETCA is still indicated, lateral exposure can be supplemented with technology including angled endoscopes and instruments, transposition of the Eustachian tube, and drilling of the jugular tubercle. 14 54 55 56 57 Despite being able to expose these lateral structures in a cadaveric setting, copious venous bleeding from the basilar venous plexus during bone removal can limit the lateral access of these approaches and, of course, careful hemostasis of any venous bleeding should be performed before continuing with the intradural portion of the dissection. 55
Inferior extension can be supplemented by detachment and anteroinferior transposition of the Eustachian–nasopharynx complex. Without any manipulation of the posterior nasopharynx, the inferior limit is approximately at the level of the of the lower clivus. If the Eustachian–nasopharynx complex is mobilized anteroinferiorly through bilateral pterygosphenoidal fissure tissue transection ( Fig. 3C ) but without incision of the posterior nasopharynx, the inferior limit of the EETCA is the upper craniocervical junction. To maximize the inferior reach of the EETCA, sharply dividing the posterior nasopharynx affords access to the C2 nerve roots. 53
Complications of the EETCAs are mainly due to the risk of injuring the paraclival ICAs, the basilar artery and its pontine perforators, and the abducens nerve in the prepontine cistern as it enters Dorello's canal. 9 27 28 42 The risk of injury to the paraclival ICAs can increase if the bone covering the ICA is removed to improve the surgical access laterally. 58 In order to reduce the risk of injury to the intracranial vessels, careful study of preoperative imaging and intraoperative Doppler ultrasound may help identify the precise location of the underlying vasculature prior to opening the dura. 27 Another drawback of the EETCAs is the increased risk of CSF leak. 28 59 To mitigate the risk of postoperative CSF leak, robust multilayered skull base reconstruction is required. For posterior fossa defects, reconstruction often includes autologous fat, fascia lata, and a pedicled nasoseptal flap. 27 28 60 61 62 63 We hypothesize that preserving the nasopharyngeal mucosa may decrease the risk of postoperative CSF leak. 22 Additionally, postoperative lumbar drainage has been shown to significantly decrease the risk of postoperative CSF leak for large posterior fossa defects. 61 62 63 Despite the advancement of techniques and the growing experience of skull base surgeons, CSF leak remains a significant issue with reported rates of 16.5% for EETCAs with multilayer reconstruction. 27
Conclusion
Mastery of the surgical steps and anatomical landmarks of the endoscopic endonasal middle and inferior clivectomies, far-medial approach, and odontoidectomy is required prior to their utilization in a clinical setting. Thus, we provide a succinct, yet comprehensive, description of the main steps and technical nuances of the EETCAs for trainees in skull base surgery.
Acknowledgments
We thank the Fondazione Beretta for their constant devotion to supporting brain cancer research.
Funding Statement
Funding This work was supported in part by Joseph I. and Barbara Ashkins Endowed Professorship in Neurosurgery and by Charles B. and Ann L. Johnson Endowed Professorship in Neurosurgery.
Conflict of Interest None declared.
Ethical Approval
This retrospective chart review study involving human participants was in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The Human Investigation Committee (IRB) of the Mayo Clinic approved this study.
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