Surgical Anatomy of the Eustachian Tube for Endoscopic Transnasal Skull Base Surgery: A Cadaveric and Radiologic Study

Original Article

Surgical Anatomy of the Eustachian Tube for Endoscopic Transnasal Skull Base Surgery: A Cadaveric and Radiologic Study Noritaka Komune1, Satoshi Matsuo2, Koichi Miki3, Yojiro Akagi4, Ryota Kurogi4, Koji Iihara4, Takashi Nakagawa1

OBJECTIVE: The endoscopic endonasal approach to the anatomically complex lateral skull base presents technical challenges. The use of the eustachian tube as a landmark to identify the petrous internal carotid artery has recently been reported, and this study aims to define the anatomic relationship between the eustachian tube and its surrounding structures using cadaveric dissection and radiologic analysis.

endonasal route. A profound understanding of the relationship between the eustachian tube and the surrounding skull base structures is important for endoscopic endonasal skull base surgeries.

METHODS: To clarify the relationship of the eustachian tube with its surrounding structures, we performed endoscopic and microscopic dissection of 4 adult cadaveric heads and analyzed computed topography scans from 20 patients.

INTRODUCTION

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RESULTS: The eustachian tube is divided into the osseous and cartilaginous parts. The cartilaginous part can be further subdivided into the posterolateral, middle, and anteromedial parts, based on its relationship to the skull base. The eustachian tube is closely related to the pterygoid process of the sphenoid bone, the foramen lacerum, and the petrosal apex and is directed away from the oblique sagittal plane almost parallel to the vidian canal at 12.2  6.2 (mean  standard deviation). The relationship between the course of the vidian canal and the eustachian tube can aid the estimation of the anatomic course of the horizontal segment of the petrous carotid artery.

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CONCLUSIONS: The eustachian tube is a useful landmark for predicting the course of the internal carotid artery when accessing the lateral skull base regions via an

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Key words - Eustachian tube - Lateral skull base - Petrous apex - Surgical anatomy Abbreviations and Acronyms 3D: Three-dimensional CTA: Computed tomography angiography

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he endoscopic endonasal approach has been applied to the lateral skull base regions and used to access the petrous apex to resect several pathogens.1-12 Previously reported approaches allow excellent access and visualization of the lateral regions and are usually performed by a skilled skull base team of otorhinolaryngologists and neurosurgeons. Recently, Shin et al.13 applied this approach to the chondrosarcoma at the petrous apex and discussed the extension of the approach to a more lateral lesion in the temporal bone. Precise three-dimensional knowledge of the skull base anatomy is required for safe endoscopic endonasal entry into the temporal bone. The vidian canal, trigeminal nerve, and eustachian tube are known as key and reliable landmarks for petrous apex lesion dissection. However, more attention has been directed to the surgical anatomy of the vidian canal and the trigeminal nerve than to the eustachian tube.5,14 To our knowledge, there remains a paucity of profound anatomic descriptions of the relationship of the eustachian tube with skull base structures. Therefore, this study focuses on elucidating the surgical anatomy of the eustachian tube. Our study used cadaveric dissection and radiologic examination to pursue the following aims: 1) to provide a detailed description of the surgical anatomy of the eustachian tube, focusing on its

Hospital Organization, Kyushu Medical Center, Fukuoka; 3Department of Neurosurgery, Graduate School of Medical Sciences, Fukuoka University, Fukuoka; and 4Department of Neurosurgery, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan To whom correspondence should be addressed: Noritaka Komune, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.01.003 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com

From the 1Department of Otorhinolaryngology, Graduate School of Medical Sciences, Kyushu University, Fukuoka; 2Department of Neurosurgery, Clinical Research Institute, National

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relationship to the skull base; 2) to clarify the importance of the eustachian tube in the endoscopic endonasal approach to the lateral skull base regions, including the petrous apex, using radiologic examination. METHODS Cadaveric Dissection Four formalin-perfused cadaveric heads were dissected to show the surgical anatomy of the eustachian tube and surrounding skull base structures. The arteries and veins were injected with a colored (red or blue) silicone rubber, Thinner 200, and RTV catalyst (Dow Corning Corp., Midland, Missouri, USA), then dissected with either a surgical microscope under 3e40X magnification, or a 0 endoscope.

Figure 1. Bone anatomy around the eustachian tube. (A) Inferior surface of the skull base. The right petrosal apex (yellow dotted line), scaphoid fossa (white dashed line), and rostral opening of the vidian canal (black arrow) are indicated. Yellow dashed line indicates the area where the cartilaginous tube attaches to the skull base, which can be divided into 3 parts. (B) View from the common nasal cavity. The insert shows the common nasal cavity of a cadaver. (C) View of the petrous apex from the nasal cavity. The insert shows the common nasal cavity of a cadaver. Car., carotid; ET, eustachian tube; Ethm., ethmoid, ethmoidal; Eust., eustachian; Fiss., fissure; For., foramen; Horiz., horizontal; Inf., inferior; Lat., lateral; Max., maxillary; Med., medial; Mid., middle; Orb., orbital; Palat., palatine; Perp., perpendicular; Pet., petrosal; Petrocliv., petroclival; Proc., process; Pteryg., pterygoid; Rost., rostrum; Scap., scaphoid; Sphen., sphenoid; Spheno., sphenoidal; Sphenopal., sphenopalatine; Sphenopet., sphenopetrosal.

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Radiologic Analysis Twenty adult patients (40 sides) from the Department of Neurosurgery at Kyushu University Hospital who underwent three-dimensional (3D) computed tomography angiography (CTA) to evaluate unruptured aneurysms that showed no masseffect intracranial lesions were included in this study. Radiologic analysis was performed by a trained neurosurgeon (S.M.) and a head and neck surgeon (N.K.). The study group consisted of 6 men and 14 women with a mean age of 62.7  11.2 years (range, 40e82 years). Patients received 100 mL of Iopamiron 370 (Nihon Bayer, Tokyo, Japan) or Omnipaque 350 (Daiichi-Sankyo, Tokyo, Japan) intravenously through an antebrachial vein at 3.0 mL/second with a powered pump, and 3D-CTA image acquisition was automatically initiated after a delay that was automatically adjusted for each patient. CTA studies for 12 patients were obtained using a 64-slice Toshiba Aquilion 64 system (Toshiba Medical Systems, Tochigi, Japan), and a 320-slice Toshiba Aquilion One system was used to acquire the CTA studies for the remaining 8 patients. We acquired 1-mm-thick 3D-CTA slice images, which were saved as DICOM (Digital Imaging and Communications in Medicine) files. The DICOM data were reconstructed and analyzed using OsiriX imaging software (version 5.9 64-bit). All images were visualized using 3D multiplanar reconstruction, and the axial and sagittal planes were confirmed to be parallel and perpendicular to the orbitomeatal line, respectively. We measured the following distances and angles: 1) the distance between the dorsal and ventral openings of the vidian canal; 2) the obtuse angle between the median sagittal plane and oblique sagittal plane parallel to the long axes of the vidian canal (plane A); 3) the obtuse angle between the median sagittal plane and oblique sagittal plane parallel to the line connecting the lateral opening of the eustachian tube and the dorsal opening of the vidian canal (plane B); 4) the acute angle between plane A and plane B; and 5) the shortest distance between the sagittal plane passing through the ventral opening of the vidian canal and the most lateral edge of the paraclival segment of the carotid artery. RESULTS In this study, we used cadaveric dissection to describe the anatomy of the skull base bones in relation to the eustachian tube (Figure 1) and the detailed surgical anatomy of the eustachian tube

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Figure 2. The course of the right eustachian tube. (A) Inferior view of the eustachian tube (yellow dashed line), which is attached to the sulcus tubae. (B) View after removal of the cartilaginous part of the eustachian tube and both pterygoid plates. (C) Removal of the pterygoid base opens the sphenoid sinus and the pterygoid canal. The long axis of the eustachian tube (white dashed line) corresponds to the line through the

Figure 3. The lateral view of the eustachian tube from the right infratemporal fossa. (A) The view of the infratemporal fossa after removal of the parotid gland, zygoma, the mandible and its related muscles, pterygoid base, and posterior wall of the maxillary sinus, with the medial pterygoid muscle and mandibular condyle left in situ. The upper part of the tensor veli palatini muscle is dissected to identify the eustachian tube. (B) Removal of the condyle exposes the neurovascular structures in the infratemporal fossa. (C) Retraction of the maxillary artery and mandibular nerve exposes the lateral surface of the eustachian tube. (D) Resection of the maxillary artery and mandibular nerve and the removal of the medial

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dorsal opening of the pterygoid canal and the medial opening of the osseous tube. A., artery; For., foramen; ICA, internal carotid artery; Inf., inferior; Infraorb., infraorbital; Lat., lateral; Lev., levator; M., muscle; Max., maxillary; Med., medial; N., nerve; Palat., palatini; Paraphar., parapharyngeal; Pet., petrosal; Proc., process; Pteryg., pterygoid; Sphen., sphenoid; Sphenopal., sphenopalatine; Sur., surface.

pterygoid muscle exposes the course of the cartilaginous part of the eustachian tube and the levator veli palatini. A., artery; Auriculo., auriculotemporal; Cond., condyle; Eust., eustachian; ICA, internal carotid artery; IJV, internal jugular vein; Lat., lateral; Lev., levator; Lig., ligament; M., muscle; Max., maxillary; Med., medial; Men., meningeal; Mid., middle; N., nerve; Palat., palatini; Petrotymp., petrotympanic; Petrosquam., petrosquamosal; Proc., process; Pteryg., pterygoid; Sphen., sphenoid; Sphenomandib., sphenomandibular; Sphenopharyng., sphenopharyngeal; Sty., styloid; Stylopharyng., stylopharyngeal; Tens., tensor; Vag., vaginal.

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Figure 4. Medial view of the relationship between the left eustachian tube and petrous apex. (A) Inferomedial view of the eustachian tube. (B) An enlarged view of (A). Detachment of the eustachian tube from the medial pterygoid plate exposes the scaphoid fossa. (C) Medial view of the eustachian tube. The insert shows the area, which is enlarged in (C) (yellow enclosed line). (D) Removal of the clivus and longus capitis shows the relationship between the petrous apex and the eustachian tube. (E) Removal of the eustachian tube exposes the sulcus tubae, which is located anterior to the petrous apex. The black arrow indicates the medial opening of the osseous part of the eustachian tube. (F) Removal of the sphenoid sinus, dura of the clivus, petroclival fissure synchondrosis, medial pterygoid

from inferior (Figure 2), lateral (Figure 3), and medial views (Figure 4). We then examined the anatomy of the eustachian tube in the context of an endoscopic endonasal transpterygoid approach (Figure 5), and further compared the surgical views provided by the infratemporal fossa approach (Figure 6) and the endoscopic endonasal approach. In addition, we used radiologic examinations of the eustachian tube to support the data generated from our cadaveric dissections (Table 1).

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muscle, and tensor and levator veli palatini muscles shows the relationship between the petrous apex and the surrounding neurovascular structures. A., artery; Car., carotid; CN, cranial nerve; Eust., eustachian; ET, eustachian tube; Fiss., fissure; For., foramen; Gang., ganglion; Hypogloss., hypoglossal; Inf., inferior; Infraorb., infraorbital; Int., internal; Lat., lateral; Lev., levator; M., muscle; Med., medial; Men., meningeal; Mid., middle; N., nerve; Optico., opticocarotid; Palat., palatini; Paracliv., paraclival; Pet., petrosal; Petrocliv., petroclival; Post., posterior; Proc., process; Pteryg., pterygoid; Rec., recess; Rosenm., Rosenmu¨ller; Rost., rostrum; Scap., scaphoid; Sphen., sphenoid; Spheno., sphenoidal; Sphenopal., sphenopalatine; Sup., superior; Synchondr., synchondrosis; Tens., tensor; Tymp., tympani.

Bone Anatomy The eustachian tube is divided into osseous and cartilaginous parts. The cartilaginous tube can be further subdivided into the following 3 parts based on its anatomic relationships to the surrounding bony structures (Figure 1A): 1) a posterolateral part related to the greater wing of the sphenoid and petrous apex; 2) a middle part related to the foramen lacerum; and 3) an anteromedial part related to the pterygoid process. The

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Figure 5. Endonasal view of endoscopic dissection of the right eustachian tube. (A) Endoscopic view of the transmaxillary transpterygoid approach. (B) The anterior genu of the internal carotid artery is reached via drilling the pterygoid base while tracing the vidian nerve. (C) Fibrocartilaginous tissue fills the space between the foramen lacerum and the eustachian tube. (D) Removal of the lateral plates and the base of the pterygoid process exposes the contents of the pterygoid fossa and scaphoid fossa.

posterolateral part of the cartilaginous part of the eustachian tube is attached to the sulcus tubae, which is roofed by the sphenopetrosal fissure between the greater wing of the sphenoid

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(E) Dissection of the medial pterygoid muscle from tensor veli palatini exposes the venous vascular space. (F, G) Separating the tensor veli palatini exposes the lateral aspect of the eustachian tube and the stylopharyngeal fascia. (H, I) The osseocartilaginous junction of the eustachian tube is located just anteromedial to the sphenoid spine and can be used as a landmark for the location of the parapharyngeal internal carotid artery. (continues)

bone and the petrous apex. The lateral edge of the sulcus tubae is continuous with the medial opening of the osseous part of the eustachian tube and is located just medial to the sphenoid

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Figure 5. (continued) (J) The endoscopic view of the entire cartilaginous eustachian tube and its relationship to the neurovascular structures of the skull base. A., artery; Acc., accessory; Ant., anterior; Car., carotid; Cav., cavernous; Chor., chorda; CN, cranial nerve; Desc., descending; Eust., eustachian; Fibrocart., fibrocartilaginous; Gang., ganglion; ICA, internal carotid artery; Inf., inferior; Infraorb., infraorbital; Int., internal; Jug., jugular; Lat., lateral; Lev., levator; Ling., lingual; M., muscle;

spine (Figure 1A). The middle part of the eustachian tube runs inferior to the sphenoid bone and anterolateral to the foramen lacerum. The anteromedial part of the eustachian tube runs inferior to the scaphoid fossa, broadly attaches to the medial pterygoid plate of the pterygoid process, and courses inferior to the vidian canal, which connects the upper medial part of the pterygopalatine fossa with the upper part of the anterolateral edge of the foramen lacerum. The medial opening of the eustachian tube is found on the lateral wall of the nasopharynx (Figure 1B). The perpendicular plate of the palatine bone and pterygoid process is located anterior and superior to the eustachian tube (Figure 1B). In the absence of the eustachian tube, the petrous apex and foramen lacerum can be observed from the common nasal meatus with a 0 endoscope in dry bone (Figure 1C). The foramen lacerum is a triangular gap

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Masset., masseteric; Max., maxillary; Med., medial; Men., meningeal; Mid., middle; N., nerve; Paracliv., palaclival; Palat., palatini; Post., posterior; Proc., process; Pteryg., pterygoid; Pterygopal., pterygopalatine; Rosenm., Rosenmu¨ller; Seg., segment; Sphen., sphenoid; Sphenomandib., sphenomandibular; Sphenopal., sphenopalatine; Stylophary., stylopharyngeal; Tens., tensor; Temp., temporal; Tymp., tympani; V., vein; Vag., vaginal.

formed by the sphenoid bone, petrous apex, and basilar part of the occipital bone (Figure 1C). Surgical Anatomy of the Eustachian Tube and Related Structures The eustachian tube runs posteriorly, laterally, and superiorly from the nasopharynx to the middle ear. Our stepwise dissection from an inferior approach showed that the long axis of the eustachian tube on the axial plane corresponds to the line passing through the medial opening of the osseous part of the eustachian tube and the dorsal opening of the vidian canal (Figure 2AeC). The eustachian tube runs almost parallel to the horizontal segment of the internal carotid artery toward the medial pterygoid plate (Figures 1A and 2AeD). Next, we exposed the eustachian tube using stepwise dissection from the lateral direction. We showed the course of the

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Figure 6. Infratemporal fossa approach for the exposure of the right eustachian tube. (A) The preauricular subtemporal infratemporal fossa approach can be used to access the osseocartilaginous junction of the eustachian tube. (B) Removal of the lateral wall of the osseous tube exposes the bony dehiscence of the medial bony wall (black arrow), which corresponds to the dehiscence of the lateral wall of the carotid canal. (C) Anterior translocation of the petrous carotid enables access to the remaining petrous bone. (D) V3 is the main structure that obscures the posterolateral

mandibular nerve and the maxillary artery in the infratemporal fossa by removing the temporal muscle, maxilla, temporomandibular joint, and lateral pterygoid muscle, which inserts into the maxillary condyle and temporomandibular joint, leaving the neurovascular structures in place (Figure 3A and B). Laterally translocating or resecting these neurovascular structures showed, in order, the medial pterygoid muscle, tensor veli palatini, levator veli palatini, and eustachian tube (Figure 3AeC). The cartilaginous part of the eustachian tube ran anteromedial to the foramen ovale (Figures 2 and 3A and B). In addition, the cartilaginous eustachian tube is not tubal and has a noncartilaginous gap located inferolaterally between the medial and lateral cartilaginous laminae (Figure 3C and D), which is covered by the tensor veli palatini, levator veli palatini, and the lateral fat pad. The tendinous membrane of the tensor veli palatini had the greatest contribution in closing the noncartilaginous gap. Resecting the tensor veli palatini and lateral fat pad enabled the observation of the lamina and the noncartilaginous gap (Figure 3). The tensor veli palatini originated from the scaphoid fossa, the sphenoid spine of the sphenoid bone, and the lateral lamina of the cartilaginous tube, ran vertically down between the medial pterygoid muscle and plate, and ended at the tendon winding around the pterygoid

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part of the cartilaginous eustachian tube. A yellow tube is inserted into the eustachian tube. A., artery; Cart., cartilaginous; Co., cochlea; Eust., eustachian; Gang., ganglion; Gasser., gasserian; Gr., greater; IAM, internal auditory meatus; ICA, internal carotid artery; Lat., lateral; Lev., levator; M., muscle; Men., meningeal; Mid., middle; N., nerve; Palat., palatini; Pet., petrosal; Post., posterior; Pteryg., pterygoid; Sphen., sphenoid; Temp., temporal; Tens., tensor; TMJ, temporomandibular joint; Tymp., tympani.

hamulus. The levator veli palatini arose from the undersurface of the apex of the petrous part of the temporal bone and was indirectly attached to the eustachian tube via only a fascial attachment to the inferior border of the medial lamina (Figure 3C and D). Next, we dissected the cadaver from the medial direction (Figure 4A). The foramen lacerum was identified superoposterior to the pharyngeal opening of the eustachian tube (Figure 4A and B). Translocating the tube inferiorly exposes the scaphoid and pterygoid fossae (Figure 4B). Removal of the clivus and longus capitis showed the petroclival and sphenopetrosal fissures. The petroclival synchondrosis was attached to the petroclival fissure and was continuous to the inferior area of the foramen lacerum and pharyngobasilar fascia. The sulcus tubae was located anterolateral to the petrosal apex (Figure 4CeE), which was located posterior to the eustachian tube (Figure 4D), and divided into anteroinferior, posteroinferior, and superior parts when viewed from an endoscopic endonasal approach.10 The superior part of the apex was located just posterior to the anterior genu and inferior to cranial nerve VI, which passes through the Dorello canal and courses through the cavernous sinus alongside the internal carotid artery (Figure 4F).

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Table 1. Measurements from Three-Dimensional Computed Tomography Angiography Data Describing the Relationship Between the Eustachian Tube and Surrounding Structures Mean (standard deviation)

Measurement 1) A distance between the dorsal and ventral openings of the vidian canal (distance A) (mm)

14.6 (2.1) 

2) An obtuse angle between the median sagittal plane and oblique sagittal plane parallel to the long axes of the vidian canal (plane A) ( )

133.4 (6.6)

3) An obtuse angle between the median sagittal plane and oblique sagittal plane parallel to the line connecting the lateral opening of the eustachian tube and the dorsal opening of the vidian canal (plane B) ( )

121.3 (44)

4) An acute angle plane A and plane B ( )

12.2 (6.2)

5) A shortest distance between the sagittal plane passing through the ventral opening the vidian canal and the most lateral edge of the paraclival segment of the carotid artery (distance B) (mm)

We examined the anatomy of the eustachian tube as observed from an endoscopic transnasal approach. Endoscopic dissection clearly showed the anatomic details of the lesion located superior and lateral to the eustachian tube. We first removed the nasal turbinates, completed an ethmoidectomy, opened the sphenoid sinus, and removed the medial and posterior walls of the maxillary sinus to expose the pterygopalatine fossa. Next, we traced the vidian nerve posteriorly to reach the anterior genu of the internal carotid artery, after crossing over the anteromedial part of the eustachian tube. The gap between the foramen lacerum and the superior surface of the eustachian tube was filled with fibrocartilaginous tissue (Figure 5B and C). Removing the base of the pterygoid process exposed the pterygoid and scaphoid fossae, which contained the attachment of the medial pterygoid and tensor veli palatini. The eustachian tube was not attached to these fossae and runs inferior to the scaphoid fossa (Figure 5D). The venous plexus was found between the medial pterygoid muscle and tensor veli palatini. However, less venous vascularity was found medial to the tensor veli palatine; thus, this plane can be used to confirm the course of the eustachian tube. The tensor veli palatini was easily separated from the lateral surface of the eustachian tube (Figure 5E and F). Lateralization of the tensor veli palatini clearly exposed the medial and lateral laminae of the cartilaginous tube and the levator veli palatini (Figure 5G). In our dissection, we found that the accessory meningeal artery passed superolateral to the tensor veli palatini and entered the skull base above the eustachian tube. We dissected the accessory meningeal artery to completely expose the attachment of the cartilaginous tube to the skull base (Figure 5H). The medial opening of the osseous part of the eustachian tube was located just medial to the sphenoid spine (Figures 1A and 5H). The vaginal process was also identified posterolateral to the attachment of the eustachian tube (Figure 5I). The stylopharyngeal fascia attached to the vaginal process covered the opening of the carotid canal and was closely related to and protects the parapharyngeal internal carotid artery, internal jugular vein, and cranial nerve IX (Figure 5H and I). Finally we exposed the entire course of the cartilaginous part of the eustachian tube (Figure 5J). The postauricular or preauricular infratemporal fossa approach can potentially be used to access the infratemporal fossa or the petrous apex.15-18 The osseous part of the eustachian tube is

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5.9 (1.6)

located just lateral to the internal carotid artery and is an important landmark for its identification during the preauricular subtemporal infratemporal fossa approach (Figure 6A). The bony dehiscence can often be observed on the medial wall of the osseous part of the eustachian tube that exposes the lateral wall of the carotid artery (Figure 6B). The osseocartilaginous junction of the eustachian tube can be exposed from the superolateral direction, and the attachment of the levator veli palatini was located just inferior to the junction (Figure 6B). The exposure of the entrance of the carotid canal could be extended by drilling into the bone between the horizontal portion of the petrous carotid and V3 and sacrificing the bony and posterolateral parts of the cartilaginous eustachian tube. A fibrocartilaginous ring was then removed to facilitate the anterior translocation of the carotid artery, which allowed us to access and drill into the remaining petrous apex (Figure 6C). Resection of the V3 was necessary to expose the entirety of the posterolateral part of the eustachian tube (Figure 6D). In contrast, the endoscopic transnasal approach enables the exposure of the eustachian tube without V3 resection, and many endoscopic approaches to the petrous apex have recently been reported.1-12 An infrapetrous approach to petrous apex required the removal of the fibrocartilaginous tissue between the foramen lacerum and eustachian tube (Figure 5B) to reach the anterior inferior petrous apex. Furthermore, to gain a wider surgical view, the eustachian tube had to be freed of its ligamentous attachments with blunt dissection and translocated inferiorly with gentle downward depression. The dissection of the tensor veli palatini from the eustachian tube allows the course of the eustachian tube to be observed without sacrificing the V3 (Figure 5H). Radiologic Study Our cadaveric dissection showed that the oblique sagittal plane through the line connecting the lateral opening of the osseous tube and the dorsal opening of the vidian canal corresponded to the plane parallel to the long axis of the eustachian tube. In our radiologic study, we confirmed that the eustachian tube runs along this plane. Knowledge of the following anatomic features is important for the safe drilling of the skull base bone in the transpterygoid approach: 1) the length of the vidian canal; 2) the direction in which the vidian canal runs; 3) the direction in which the

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horizontal segment of the internal carotid artery runs (i.e., almost parallel and anterior to the eustachian tube); and 4) the extent to which the paraclival internal carotid artery protrudes medially. Thus, we took the following measurements: 1) the distance between the dorsal and ventral openings of the vidian canal (distance A); 2) the obtuse angle between the median sagittal axial plane and the oblique sagittal plane parallel to the long axis of the vidian canal (plane A); 3) the obtuse angle between the median sagittal axial plane and the oblique sagittal plane parallel to the line connecting the lateral opening of the eustachian tube and the dorsal opening of the vidian canal (plane B); 4) the acute angle between plane A and plane B; and 5) the shortest distance between the sagittal plane passing through the ventral opening of the vidian canal and the most lateral point of the paraclival segment of the carotid artery (distance B). The results are given in Table 1. DISCUSSION The first report of an endonasal endoscopic approach to access a giant cholesterol cyst of the petrous apex was published in 1994 by Fucci et al.19 Two main routes for the endonasal approach to the petrous apex have been described: 1) the medial transsphenoid approach and 2) the transpterygoid infrapetrous approach.7,10-13 Injury of the petrous carotid artery is the most disastrous complication encountered in both approaches. Compared with the vidian and the maxillary nerves, few studies on the surgical anatomy of the eustachian have been reported.20-22 After detection of the vidian canal on the floor of the sphenoid sinus or on the base of the pterygoid process, drilling should proceed posteriorly along the inferior and medial aspects of the vidian canal toward the anterior genu of the petrous carotid, because the carotid artery is located superiorly to the vidian canal.23,24 The length of the vidian canal averaged 14.6 mm  2.1 mm (mean  standard deviation). Corroborating the results of previous studies, we did not observe carotid arteries located inferior to the vidian canal.25,26 Once the anterior genu of the petrous carotid is identified, the bone around the petrous apex and clivus can be removed laterally and posteriorly. The paraclival segment ascends within 5.9  1.6 mm away from the sagittal plane passing through the ventral opening of the vidian canal; therefore, care should be taken to avoid carotid artery injury when drilling into the clivus and the posterior wall of the sphenoid sinus within this area. Exposing the paraclival and petrous segments of the carotid artery allows proximal and distal control of the carotid artery.27 In cases in which the carotid encasement is diagnosed, or when carotid displacement is necessary during carotid encroachment, the bone surrounding the carotid artery should be skeletonized and removed.25 Intraoperative prediction of the course of the carotid artery is necessary to safely drill into the petrous apex and avoid carotid artery injury. Our cadaveric and radiologic examination shows that

REFERENCES 1. Carlton DA, Iloreta AM, Chandrasekhar SS. Endoscopic-assisted transmastoid decompression of petrous apex cholesterol granuloma. Laryngoscope. 2017;127:496-499.

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the petrous carotid courses almost parallel to the sulcus tubae and is located superomedial to the eustachian tube, which is directed away from the oblique sagittal plane parallel to the vidian canal at 12.2  6.2 . On accessing the ventral opening of the vidian canal, we can infer the course of the horizontal segment of the petrous carotid based on the course of the vidian canal and the angle between the eustachian tube and the canal. Sughrue et al.28 described the operative nuances regarding the endonasal approach to the petrous apex. These investigators reported that the eustachian tube was freed via blunt dissection of the surrounding soft tissue and ligamentous attachments and gentle downward depression of the eustachian tube and that the infrapetrous lesion could be accessed after exposure of the petroclival junction. Paluzzi et al.7 reported that the infrapetrous approach requires some degree of dissection of the eustachian tube and drilling of the petrous apex inferior to the horizontal segment of the petrous carotid. Surprisingly, the lateral limit of the endonasal endoscopic approach has been extended to the jugular tubercle, jugular fossa, internal auditory canal, and the posterior vertical segment of the internal carotid artery.7,10-13 However, the number of cases studied in these promising reports is limited; therefore, the lateral limit of these approaches is still controversial.13,29,30 Endoscopic endonasal approaches to lateral skull base lesions are extremely challenging, and the vidian nerve and V2 are known landmarks in these approaches. As shown in this study and previous reports, the eustachian tube is also an easily identifiable and readily available landmark. Anatomic dissections supported by our radiologic data would aid surgeons to successfully perform this challenging approach. The importance of using the eustachian tube as a landmark cannot be overemphasized in avoiding disastrous complications when accessing lesions lateral to the nasal cavity.

CONCLUSIONS This study reports the importance of the eustachian tube as a landmark for predicting the course of the internal carotid artery in the endoscopic endonasal approach to the lateral skull base. Avoiding disastrous complications requires an understanding of the relationship between the eustachian tube and its surrounding structures, and our cadaveric dissection and radiologic examination prove that the entire eustachian tube can be used as anatomic landmarks in this challenging approach.

ACKNOWLEDGMENTS The authors would like to express their deep gratitude to the late Professor Albert L. Rhoton, Jr., University of Florida, for giving us the opportunity to study the microsurgical anatomy of the eustachian tube in cadaveric specimens.

2. Emanuelli E, Ciorba A, Bianchini C, Bossolesi P, Stomeo F, Pelucchi S. Transnasal endoscopic management of petrous apex and clivus selected lesions. Eur Arch Otorhinolaryngol. 2013;270:1747-1750.

combined microscopic surgery and an adjuvant endoscopic approach. J Neurol Surg Rep. 2016;77: e46-e49.

3. Iannella G, Savastano E, Pasquariello B, Re M, Magliulo G. Giant petrous bone cholesteatoma:

4. Jen A, Sanelli PC, Banthia V, Victor JD, Selesnick SH. Relationship of petrous temporal

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bone pneumatization to the eustachian tube lumen. Laryngoscope. 2004;114:656-660. 5. Kassam AB, Vescan AD, Carrau RL, Prevedello DM, Gardner P, Mintz AH, et al. Expanded endonasal approach: vidian canal as a landmark to the petrous internal carotid artery. J Neurosurg. 2008;108:177-183. 6. Kumral TL, Uyar Y, Yildirim G, Berkiten G, Mutlu AT, Kilic MV. Does endoscopic surgery reduce recurrence of the petrous apex cholesteatoma? Indian J Otolaryngol Head Neck Surg. 2013; 65:327-332. 7. Paluzzi A, Gardner P, Fernandez-Miranda JC, Pinheiro-Neto CD, Scopel TF, Koutourousiou M, et al. Endoscopic endonasal approach to cholesterol granulomas of the petrous apex: a series of 17 patients: clinical article. J Neurosurg. 2012;116: 792-798. 8. Patron V, Hitier M. In reference to endoscopicassisted transmastoid decompression of petrous apex cholesterol granuloma. Laryngoscope. 2017; 127:E209-E210. 9. Presutti L, Alicandri-Ciufelli M, Rubini A, Gioacchini FM, Marchioni D. Combined lateral microscopic/endoscopic approaches to petrous apex lesions: pilot clinical experiences. Ann Otol Rhinol Laryngol. 2014;123:550-559. 10. Scopel TF, Fernandez-Miranda JC, PinheiroNeto CD, Peris-Celda M, Paluzzi A, Gardner P, et al. Petrous apex cholesterol granulomas: endonasal versus infracochlear approach. Laryngoscope. 2012;122:751-761. 11. Taniguchi M, Akutsu N, Mizukawa K, Kohta M, Kimura H, Kohmura E. Endoscopic endonasal translacerum approach to the inferior petrous apex. J Neurosurg. 2016;124:1032-1038. 12. Zanation AM, Snyderman CH, Carrau RL, Gardner PA, Prevedello DM, Kassam AB. Endoscopic endonasal surgery for petrous apex lesions. Laryngoscope. 2009;119:19-25. 13. Shin M, Kondo K, Hanakita S, Hasegawa H, Yoshino M, Teranishi Y, et al. Endoscopic transsphenoidal anterior petrosal approach for locally aggressive tumors involving the internal auditory canal, jugular fossa, and cavernous sinus. J Neurosurg. 2017;126:212-221.

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Conflict of interest statement: This work was supported by the University of Florida Foundation. Received 21 October 2017; accepted 3 January 2018

23. Liu J, Pinheiro-Neto CD, Fernandez-Miranda JC, Snyderman CH, Gardner PA, Hirsch BE, et al. Eustachian tube and internal carotid artery in skull base surgery: an anatomical study. Laryngoscope. 2014;124:2655-2664. 24. Ozturk K, Snyderman CH, Gardner PA, FernandezMiranda JC. The anatomical relationship between

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