Anatomical nuances of the internal carotid artery in relation to the quadrangular space

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OBJECTIVE

The aim of this study was to evaluate the anatomical variations of the internal carotid artery (ICA) in relation to the quadrangular space (QS) and to propose a classification system based on the results.

METHODS

A total of 44 human cadaveric specimens were dissected endonasally under direct endoscopic visualization. During the dissection, the anatomical variations of the ICA and their relationship with the QS were noted.

RESULTS

The space between the paraclival ICAs (i.e., intercarotid space) can be classified as 1 of 3 different shapes (i.e., trapezoid, square, or hourglass) based on the trajectory of the ICAs. The ICA trajectories also directly influence the volumetric area of the QS. Based on its geometry, the QS was classified as one of the following: 1) Type A has the smallest QS area and is associated with a trapezoid intercarotid space, 2) Type B corresponds to the expected QS area (not minimized or enlarged) and is associated with a square intercarotid space, and 3) Type C has the largest QS area and is associated with an hourglass intercarotid space.

CONCLUSIONS

The different trajectories of the ICAs can modify the area of the QS and may be an essential parameter to consider for preoperative planning and defining the most appropriate corridor to reach Meckel's cave. In addition, ICA trajectories should be considered prior to surgery to avoid injuring the vessels.

ABBREVIATIONS CN = cranial nerve; CSF = cerebrospinal fluid; EEA = endoscopic endonasal approach; ICA = internal carotid artery; QS = quadrangular space.

OBJECTIVE

The aim of this study was to evaluate the anatomical variations of the internal carotid artery (ICA) in relation to the quadrangular space (QS) and to propose a classification system based on the results.

METHODS

A total of 44 human cadaveric specimens were dissected endonasally under direct endoscopic visualization. During the dissection, the anatomical variations of the ICA and their relationship with the QS were noted.

RESULTS

The space between the paraclival ICAs (i.e., intercarotid space) can be classified as 1 of 3 different shapes (i.e., trapezoid, square, or hourglass) based on the trajectory of the ICAs. The ICA trajectories also directly influence the volumetric area of the QS. Based on its geometry, the QS was classified as one of the following: 1) Type A has the smallest QS area and is associated with a trapezoid intercarotid space, 2) Type B corresponds to the expected QS area (not minimized or enlarged) and is associated with a square intercarotid space, and 3) Type C has the largest QS area and is associated with an hourglass intercarotid space.

CONCLUSIONS

The different trajectories of the ICAs can modify the area of the QS and may be an essential parameter to consider for preoperative planning and defining the most appropriate corridor to reach Meckel's cave. In addition, ICA trajectories should be considered prior to surgery to avoid injuring the vessels.

ABBREVIATIONS CN = cranial nerve; CSF = cerebrospinal fluid; EEA = endoscopic endonasal approach; ICA = internal carotid artery; QS = quadrangular space.

A surge in the use of endoscopy during skull base surgery, especially for transsphenoidal pituitary surgery, along with increases in the number of anatomical studies, neurophysiological monitoring, collaboration between skull base surgeons, and technological advances, has contributed to the development of extended endoscopic endonasal approaches (EEAs).3–5,30–32 These extended techniques provide appropriate exposure of the lesion with minimal manipulation of the brain, blood vessels, and cranial nerves. Early promising outcomes have increased the number of indications for EEAs in the management of lesions involving the ventral skull base, thereby becoming an alternative to traditional transcranial and craniofacial approaches in select patients. The introduction of EEAs combined with the development of the nasoseptal flap closure technique has resulted in decreased surgical morbidity and dramatically reduced postoperative cerebrospinal fluid (CSF) leaks.9,13,19,23–26,30,31,39

Meckel's cave, also known as the “trigeminal cave,” is a diverticulum in the middle cranial fossa, formed by the splitting of the 2 layers of the dura mater.25,36 The limits of Meckel's cave are formed by the meningeal layer of the dura mater that covers the middle fossa superolaterally and by the periosteal layer in the temporal fossa and petrous carotid canal inferomedially.21,25,38,42

Several transcranial techniques have been described to access lesions in this region. These approaches can be divided into 3 major groups: anterolateral, posterolateral, and lateral.21,35,36,38,40,42 Unfortunately, all transcranial approaches present a similar limitation; they fail to provide access to the anteromedial aspect of Meckel's cave, which is guarded by the trigeminal nerve when coming from a lateral approach. They also have the potential for morbidity related to the retraction and manipulation of brain tissue, important vessels, and cranial nerves that are present within the surgical corridor.25 Therefore, developing alternatives to the classic transcranial approaches to Meckel's cave is desirable. This region can be affected by several pathologies; however, the most common are schwannomas of the trigeminal nerve and meningiomas.27,41,43 Less common lesions include chordomas, chondrosarcomas, epidermoid cysts, and sinonasal malignancies.11,15,18,43,44

In 2009, Kassam et al. described an EEA that provides a direct route to the anteromedial region of Meckel's cave.25 The main advantage of this technique lies in facilitation of the dissection between the trigeminal nerve and the periosteal layer of the dura mater, allowing access to lesions in the anteromedial portion of Meckel's cave. Kassam and colleagues demonstrated that rates of morbidity associated with this approach are satisfactorily low. Access is achieved through the quadrangular space (QS), which was named the “front door of Meckel's cave.”25 Entry into this space is limited medially and inferiorly by the internal carotid artery (ICA). Therefore, this technique, in combination with transcranial approaches, gives the skull base surgeon the potential to access 360° of Meckel's cave.

Injury to the ICA is one of the most disastrous complications that can occur during microscopic transsphenoidal surgery or EEAs.12,16 An ICA injury can lead to death, postoperative pseudoaneurysm or mycotic aneurysm, vasospasm, vascular occlusion, or carotid-cavernous fistula. The rate of ICA injury by novice surgeons varies from 0.4% to 1.4%, but rates of injury to the parasellar segment of the ICA have been reported to be as high as 3.8%.7,8,29 To avoid this complication, a thorough knowledge of ICA anatomy is mandatory.

Widely used classification schemes for ICA anatomy, such as those proposed by Gibo et al.,17 Rhoton,33,34 and Bouthillier et al.,2 are more useful when employing a classic transcranial microscopic approach. However, when using an EEA, the surgeon has a different ventral perspective of the ICA and adjacent regions. Optical characteristics of the endoscope, including its bidimensional view and barrel-type distortions, add further challenges to mastering this anatomy. Descriptions of ICA anatomy based on the endoscopic endonasal view have come to light only recently.1,10,14,20,29 Different anatomical presentations of the ICA, especially those of the paraclival and parasellar segments, may alter the QS geometry and increase the risk for an ICA injury during an approach to Meckel's cave. Therefore, a better understanding of ICA anatomical variations and their relationship with the QS is mandatory.

Methods

This study received an institutional review board exemption, as dissections were performed on de-identified cadaveric specimens. However, the Anatomy Laboratory Toward Visuospatial Surgical Innovations in Otolaryngology and Neurosurgery (ALT-VISION) at the Wexner Medical Center at The Ohio State University and its researchers are certified by regulatory agencies in dealing with the use of human tissues and cadaveric studies.

Forty-four fresh human cadaveric specimens (88 sides) were prepared with intravascular injection of colored silicone through the ICAs and internal jugular veins.37 The specimens were stored in 70% alcohol throughout the duration of the project. Cadaveric specimens were dissected via the endoscopic approach bilaterally.

The surgical dissection was performed using paranasal sinus and skull base neurosurgical endoscopic instruments (Karl Storz Endoscopy) and a combination of straight high-speed drills (Stryker Corp.) and angled-handpiece high-speed drills (Medtronic), both with coarse diamond cutting burs. All dissections were performed using a pure EEA with a 0°, 30°, and 45° rodlens endoscope coupled to a high-definition camera and monitor (Karl Storz Endoscopy).

In all specimens, dissection of the ICA was performed bilaterally, extending from the first genu (petrous portion of the ICA) to the clinoid segment of the ICA (i.e., including the segments associated with the QS and the cavernous sinus; Figs. 1 and 2). The shape and course of the ICA in this portion were documented, and its relationship with the QS was analyzed. This information was used to demonstrate how variations in the ICA trajectory altered the QS area and geometry.

FIG. 1.
FIG. 1.

EEA with a 0° endoscope (A, B, and C) and 30° endoscope (D, E, and F) showing the stepwise cadaveric dissection of the pterygopalatine fossa and cavernous sinus. A: Essential landmarks in an endoscopic endonasal skull base surgery are identified. This dissection was performed through a wide antrostomy exposing the posterior wall of the maxillary sinus; behind the bone it is possible to visualize the right infraorbital artery and its corresponding nerve going upward toward the right orbit. Superiorly and posteriorly, the lamina papyracea can be identified. Medially and superiorly to the lamina papyracea, located in the midline, is the cribriform plate, a critical structure in the surgical dissection to reach the anterior fossa. Inferiorly and posteriorly to the cribriform plate, also in the midline, 2 essential landmarks can be visualized: the sella and the clivus. B: Using a ball probe, we performed a dissection between the mucosa and the bone to expose the sphenopalatine foramen; this is a key landmark to identify since it contains the nasoseptal artery that provides blood supply to the nasoseptal flap, which has revolutionized endoscopic endonasal skull base surgery. Inferiorly and medially to the sphenopalatine foramen, the eustachian tube is located. C: A closer view of the sphenopalatine foramen and infraorbital nerve and its corresponding artery in the posterior wall of the maxillary sinus. D: The bone from the posterior wall of the maxillary sinus was removed to give access to the pterygopalatine fossa. The first identifiable layer is the periosteum. E: The bone and periosteum were removed to visualize some branches of the maxillary artery located in the pterygopalatine fossa. Lateral to the pterygopalatine fossa is the infratemporal fossa. The major terminal branch of the external carotid arteries is the maxillary artery that will give several branches; the most important one for skull base surgeons is the sphenopalatine artery. Other branches that can be visualized are the descending palatine artery and the posterior superior alveolar artery. Lateral to these structures is the temporal muscle in the infratemporal fossa. In the first plane it is possible to identify the arteries and the nerves behind it. In this figure panel we can also see the infraorbital nerve, which is an extension of the maxillary nerve after it crosses the foramen rotundum. F: The last step in the dissection of the lateral wall of the cavernous sinus and the QS. The vidian nerve was dissected in its entire pathway, starting from the pterygopalatine ganglion, which was removed, and ending in the foramen lacerum. On the lateral wall of the cavernous sinus are cranial nerve (CN) III, CNV1, CNV2, and the entire course of CNVI. The ICA was exposed from the foramen lacerum to the intracranial segment; therefore, after this dissection we can observe all the structures that compose the QS borders. AM = anteromedial; CNIII = oculomotor nerve; CNV1 = ophthalmic nerve; CNV2 = maxillary nerve; CNV3 = mandibular nerve; CNVI = abducens nerve; CP = cribriform plate; DPA = descending palatine artery; ET = eustachian tube; FR = foramen rotundum; Imax = internal maxillary artery; IOA = infraorbital artery; ION = infraorbital nerve; LP = lamina papyracea; pcICA = paraclival segment of ICA; PP = pterygoid process; PS = planum sphenoidale; PSAA = posterior superior alveolar artery; psICA = parasellar segment of ICA; PwMS = posterior wall of maxillary sinus; SPA = sphenopalatine artery; SPF = sphenopalatine foramen; TM = temporal muscle; VN = vidian nerve.

FIG. 2.
FIG. 2.

Detailed 0° (A, B, and F) and 30° (C, D, and E) endoscopic views of the QS and surrounding structures. A: The bone on the right and left side of the lateral wall of the sphenoid sinus was removed. The dura was removed on the right side, allowing visualization of CNVI and the paraclival and parasellar segments of the ICA. On the left side, the dura was kept intact, and the lateral opticocarotid recess is visible superiorly; this is a critical landmark to recognize between the optic nerve and ICA; inferiorly, from lateral to medial, it is visualized by the impression of the maxillary strut and the maxillary nerve behind the dura. The portion of bone that was preserved in front of the QS, working like a shield to protect it, we named the “QS strut.” B: The QS strut was removed. C: With a 30° endoscope, the entire course of the vidian nerve can be seen along the vidian canal. It is possible to visualize the lateral recess of the sphenoid sinus, a space between the vidian nerve and the maxillary nerve. The dura around the lateral opticocarotid recess was removed to show the relationship between the parasellar segment of the ICA and the optic nerve. D: With the 30° endoscope, more details of the impression of the QS strut in the dura are visible. E: The dura around the paraclival segment of the ICA was removed, allowing a closer view of the vidian canal, lateral recess of the sphenoid sinus, and the impression of the maxillary nerve. F: The area around the QS in more detail; the sympathetic nerve fibers running with the paraclival segment of the ICA are visible, leaving it to join to the abducens nerve. CNII = optic nerve; iMS = impression of maxillary strut; iQSS = impression of QS strut; LOCR = lateral opticocarotid recess; LRSS = lateral recess of sphenoid sinus; QSS = QS strut; SF = sympathetic fibers; SS = sphenoid sinus; TS = tuberculum sellae; VC = vidian canal.

Our study used the ICA angle classification scheme proposed by Cebula et al.,6 which categorizes the angle between the parasellar and paraclival segments of the ICA into 4 types: < 80° (Type I), 80°–100° (Type II), > 100° (Type III), and asymmetrical (Type IV). All analyses and measurements were performed using Adobe Acrobat Pro software (version 11.0).

Results

ICA Angle Measurements

Forty-four cadaveric specimens (88 sides) were analyzed using the aforementioned classification scheme introduced by Cebula et al.,6 which is based on the size of the angle formed by the paraclival and parasellar segments of the ICA (Fig. 3B).

FIG. 3.
FIG. 3.

Illustrations and anatomical dissection demonstrating the different ICA angles, their relation with the QS, and our proposed QS classification scheme. A: Illustration depicting a ventral perspective of an EEA. On the left, note the shadow of the right sphenoid bone and its corresponding superior orbital fissure and nerves; the nerves passing through the superior orbital fissure from superior to inferior are (in order) the lacrimal nerve, frontal nerve (a branch of the ophthalmic nerve), trochlear nerve (CNIV), superior division of the oculomotor nerve (CNIII), nasociliary nerve (a branch of the ophthalmic nerve), inferior division of the oculomotor nerve (CNIII), and the abducens nerve (CNVI). Superior to the superior orbital fissure, it is possible to identify the optic nerve and ophthalmic artery entering the optic canal. In addition, several anatomical structures and their relations are illustrated (superior to inferior); the optic chiasm is located superiorly, and lateral to it is CNII. Inferior to the chiasm is the pituitary stalk, which connects to the hypophysis. In the background, inferior to the pituitary gland, the vertebral arteries join themselves to form the basilar artery. The petrous, paraclival, parasellar, paraclinoid, and intradural segments of the left ICA are exposed. Lateral to the left ICA (superior to inferior) are CNII, CNIII, CNIV, CNV1, CNVI, CNV2, and CNV3. The QS is highlighted in blue. This is an area limited medially by the paraclival ICA, inferiorly by the horizontal petrous ICA, laterally by CNV2, and superiorly and obliquely by CNVI. B: Illustrations depicting the different types of ICA angle measurements on the right ICA. This classification scheme, proposed by Cebula et al., 2014, categorizes the angle between the parasellar and paraclival ICA segments into 1 of 4 types: < 80° (Type I), 80°–100° (Type II), > 100° (Type III), and asymmetrical (Type IV). The intercarotid space classification is highlighted in green. The intercarotid space is located between the parasellar and paraclival segments of both ICAs and is categorized based on its shape. The trapezoid shape is created when the course of the parasellar to paraclival segments of the ICA runs medial to lateral. With this type of intercarotid space, the distance between the ICAs in this trajectory (superior to inferior) widens. The square shape is created when the course of the parasellar to paraclival segments of the ICA is straight. The distance between the ICAs in this trajectory (superior to inferior) remains the same. The hourglass shape is created when the course of the parasellar to paraclival segments of the ICA is lateral to medial. The distance between the ICAs in this trajectory (superior to inferior) narrows. Our proposed QS classification is highlighted in blue. The QS is considered to be Type A when the shape of the intercarotid space (green) is trapezoid; the area and shape of the QS becomes narrower and shorter. The QS is considered to be Type B when the shape of the intercarotid space is square; the shape and area of the QS does not significantly alter. The QS is considered to be Type C when the intercarotid space has an hourglass shape; the area and shape of the QS becomes wider and longer. Images of cadaveric dissection of the left ICA, performed through an EEA using a 0° endoscope, mimic the illustrations. CNIV = trochlear nerve. Illustrations by Anthony Baker. Copyright The Ohio State University. Published with permission.

Intercarotid Space

We classified the space between the paraclival segments of the left and right ICA as 1 of 3 shapes, namely trapezoid, square, or hourglass (Fig. 3). Each ICA was analyzed separately, allowing us to define which type of ICA angle variation is more frequent for each particular intercarotid space shape (Table 1 and Figs. 4 and 5).

TABLE 1.

Relationship between ICA angle type and shape of intercarotid space

ICA Angle TypeShape of Intercarotid SpaceTotal
TrapezoidSquareHourglass
Type I168024 (27%)
Type II2226 (7%)
Type III4142240 (46%)
Type IV*Type I: 3Type I: 2Type I: 018 (20%)
Type II: 1Type II: 2Type II: 1
Type III: 4Type III: 4Type III: 1
Total30 (34%)32 (36%)26 (30%)88 (100%)

Type IV ICAs are divided because they can exhibit a different angle on each side.

FIG. 4.
FIG. 4.

Illustration depicting the distribution of ICA angle types in 44 cadaveric specimens (88 sides). The classification scheme developed by Cebula et al., based on the angle between the paraclival and parasellar segments of the ICA, was used. Twelve cadaveric specimens (27%) displayed a Type I angle, in which the angle between the paraclival and parasellar segments of the ICA is < 80° bilaterally. Three specimens (7%) displayed a Type II angle, in which the angle between the paraclival and parasellar segments of the ICA is 80°–100° bilaterally. Twenty specimens (46%) displayed a Type III angle, in which the angle between the paraclival and parasellar segments of the ICA is > 100° bilaterally. Nine specimens (20%) displayed a Type IV angle, in which the angle between the paraclival and parasellar segments of the ICA has a different type on each side.

FIG. 5.
FIG. 5.

Graph depicting the relationship between ICA angle type and shape of the intercarotid space. A Type I angle (< 80°) was most commonly found in the 15 cadaveric specimens (34%) with a trapezoid-shaped intercarotid space. A Type III angle (> 100°) was most frequently found in the 16 cadaveric specimens (36%) with a square (straight)–shaped intercarotid space. A Type III angle (> 100°) was most commonly found in 13 cadaveric specimens (30%) with an hourglass-shaped intercarotid space. No Type I angles were observed with this conformation.

Relationship Between ICA Measurement Angles and Intercarotid Space

Each ICA was analyzed individually since Type IV ICAs can exhibit a different angle on each side. The trapezoid shape was found in 15 cadaveric specimens (30 ICAs), the square shape was found in 16 (32 ICAs), and the hourglass shape was found in 13 (26 ICAs; Table 1 and Fig. 5).

A total of 29 Type I angles were analyzed individually. In 11 cadaveric specimens, the angle between the paraclival and parasellar segments of the ICA was found to be less than 50°; in these cases, it was not possible to visualize the proximal segment of the abducens nerve (cranial nerve [CN] VI, located at the superior border of the QS), as it was situated below the parasellar segment of the ICA. In the remaining 18 cases, the angle was between 50° and 80°, allowing visualization of the entire pathway of CN VI.

QS Classification

The relationship between shape of the intercarotid space (trapezoid, square, or hourglass) and QS area was noted during our analysis. Using this information, we propose the following classification scheme for types of QS.

  • Type A: when the shape of the intercarotid space is trapezoid, the paraclival to parasellar segments of the ICA (proximal to distal) run lateral to medial. In this situation, the area and shape of the QS becomes narrower and shorter.
  • Type B: when the shape of the intercarotid space is square, the paraclival to parasellar segments of the ICA (proximal to distal) run straight. In this situation, the shape and area of the QS does not present a significant alteration.
  • Type C: when the intercarotid space has an hourglass shape, the paraclival to parasellar segments of the ICA (proximal to distal) run medial to lateral. In this situation, the area and shape of the QS becomes wider and longer (Fig. 3B).

Discussion

Several classification schemes describe ICA trajectories; however, the majority are described in relation to open transcranial approaches,2,17,33,34 and only recently have ICA classifications focusing on the ventral perspective been proposed.1,10,14,20 This study adopted the ICA classification system proposed by Labib and colleagues22,28,29 and the ICA angle classification created by Cebula et al.6

Measurements of ICA angles in our study (prevalence of Type I, II, III, and IV angles was 27%, 7%, 46%, and 20%, respectively; Table 1) were similar to those of Cebula and colleagues (25%, 35%, 15%, and 25%, respectively).6 The prevalence of Type I and IV angles was very similar in the 2 studies. Although there was a discrepancy between the 2 studies in the prevalence of Type II and III angles, we found that they account for similar rates when the 2 angle types are merged (53% total for Types II and III in our study and 50% in Cebula's study). It is possible to analyze Type II and III angles together as they do not present significant differences when comparing the intercarotid space and QS classification.

Our study suggests that the trapezoid-shaped intercarotid space was more commonly associated with Type I ICA angles (when the angle between the parasellar and paraclival ICA segment is < 80°), the square intercarotid space was associated with Type III ICA angles (when the angle between the parasellar and paraclival ICA segment is > 100°), and the hourglass-shaped intercarotid space was associated with Type III ICA angles (88% of Type III angles were found with an hourglass intercarotid space). Cebula et al.6 noted identical relationships for the trapezoid- and hourglass-shaped intercarotid spaces; the square intercarotid space was not described in their publication (36% had the square-shaped intercarotid space).

Our analysis revealed an important relationship between the intercarotid space and the QS. When the intercarotid space is trapezoid-shaped, it means that the paraclival segment of the ICA courses to the parasellar segment (proximal to distal) from lateral to medial, so the QS becomes narrow and short (Type A). When the shape of the intercarotid space is square, the course of the paraclival to the parasellar segment of the ICA (proximal to distal) is straight; thus, the QS does not suffer any significant alteration (Type B). Finally, when the intercarotid space is hourglass-shaped, the paraclival segment of the ICA courses to the parasellar segment (proximal to distal) from medial to lateral. In this situation, the QS becomes larger and greater (Type C).

These results are valuable in preoperative planning to access the QS, its surroundings, and the ICA itself. It is hard to visualize the QS directly with imaging studies; however, by evaluating ICA trajectories and the shape of the intercarotid space, we are able to predict how they will affect the QS intraoperatively. This can enable surgeons to avoid any iatrogenic ICA injury during surgery.

In our study, we demonstrate that surgical access to a Type C QS (hourglass-shaped intercarotid space) is easier since the area of the “front door” will be wider. It is also possible to note that the distance between the paraclival segments of the ICAs is shorter than in trapezoid- and square-shaped intercarotid spaces. Conversely, a Type A QS (trapezoid-shaped) is associated with more challenging access to Meckel's cave.

When analyzing the ICA angle measurements, we observed that in 11 cadaveric specimens with a Type I angle (< 80°), the angle was less than 50°. This hampered visualization of the proximal segment of CN VI, as the nerve was hidden behind the parasellar segment of the ICA. The distal segment was visible after it crossed the ICA, traveling anteriorly and obliquely toward the superior orbital fissure. CN VI defines the superior border of the QS; thus, in these specimens it was not possible to visualize the entire limits of the “front door.” It is important to understand the exact localization of CN VI to avoid any iatrogenic lesions. Intraoperative neurophysiological monitoring helps to locate and protect the nerve during surgery, but this becomes more difficult when the nerve is located below the parasellar ICA.

It is important to highlight that the findings in this study are described in normal structures and the anatomical variations naturally occurring in ICAs and the QS. When a tumor grows in this area, there may be variable anatomical distortions caused by the mass. Nonetheless, knowledge of this region is of the utmost importance as it offers information that can be used in preoperative planning to minimize possible complications.

Conclusions

Different possible trajectories of the ICAs can modify the QS and may be an essential parameter for preoperative planning and selecting the most appropriate route to reach Meckel's cave. Anatomical knowledge of this region and its variations is critical to avoid iatrogenic lesions and further complications.

Acknowledgments

Dr. Dolci is sponsored by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) from Brazil.

Disclosures

The authors report no conflict of interest concerning the materials and methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Prevedello, Dolci, Lazarini. Acquisition of data: Dolci. Analysis and interpretation of data: Prevedello, Dolci. Drafting the article: Dolci, Upadhyay, Buohliqah, Carrau. Critically revising the article: Prevedello, Carrau. Reviewed submitted version of manuscript: Prevedello. Approved the final version of the manuscript on behalf of all authors: Prevedello. Administrative/technical/material support: Ditzel Filho, Goulart, Upadhyay. Study supervision: Prevedello, Lazarini, Carrau.

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    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Herzallah IRCasiano RR: Endoscopic endonasal study of the internal carotid artery course and variations. Am J Rhinol 21:2622702007

  • 21

    Inoue TRhoton AL JrTheele DBarry ME: Surgical approaches to the cavernous sinus: a microsurgical study. Neurosurgery 26:9039321990

  • 22

    Kassam ALabib MAPrevedello DMCarrau R: In reply: An endoscopic roadmap of the internal carotid artery. Neurosurgery 77:E154E1552015. (Letter)

    • Search Google Scholar
    • Export Citation
  • 23

    Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part I. Crista galli to the sella turcica. Neurosurg Focus 19:1E32005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part II. Posterior clinoids to the foramen magnum. Neurosurg Focus 19:1E42005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Kassam ABPrevedello DMCarrau RLSnyderman CHGardner POsawa S: The front door to Meckel's cave: an anteromedial corridor via expanded endoscopic endonasal approach—technical considerations and clinical series. Neurosurgery 64:3 Supplons71ons832009

    • Search Google Scholar
    • Export Citation
  • 26

    Kassam ABPrevedello DMCarrau RLSnyderman CHThomas AGardner P: Endoscopic endonasal skull base surgery: analysis of complications in the authors' initial 800 patients. J Neurosurg 114:154415682011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Kouyialis ATStranjalis GPapadogiorgakis NPapavlassopoulos FZiaka DSPetsinis V: Giant dumbbell-shaped middle cranial fossa trigeminal schwannoma with extension to the infratemporal and posterior fossae. Acta Neurochir (Wien) 149:9599642007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Kurbanov AZimmer LATheodosopoulos PVLeach JLKeller JT: An endoscopic roadmap of the internal carotid artery. Neurosurgery 77:E153E1542015. (Letter)

    • Search Google Scholar
    • Export Citation
  • 29

    Labib MAPrevedello DMCarrau RKerr EENaudy CAbou Al-Shaar H: A road map to the internal carotid artery in expanded endoscopic endonasal approaches to the ventral cranial base. Neurosurgery 10:Suppl 34484712014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Mascarenhas LMoshel YABayad FSzentirmai OSalek AALeng LZ: The transplanum transtuberculum approaches for suprasellar and sellar-suprasellar lesions: avoidance of cerebrospinal fluid leak and lessons learned. World Neurosurg 82:1861952014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Prevedello DMDitzel Filho LFSolari DCarrau RLKassam AB: Expanded endonasal approaches to middle cranial fossa and posterior fossa tumors. Neurosurg Clin N Am 21:621635vi2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Prevedello DMDoglietto FJane JA JrJagannathan JHan JLaws ER Jr: History of endoscopic skull base surgery: its evolution and current reality. J Neurosurg 107:2062132007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Rhoton AL Jr: The cavernous sinus, the cavernous venous plexus, and the carotid collar. Neurosurgery 51:4 SupplS375S4102002

  • 34

    Rhoton AL Jr: The supratentorial arteries. Neurosurgery 51:4 SupplS53S1202002

  • 35

    Samii MCarvalho GATatagiba MMatthies C: Surgical management of meningiomas originating in Meckel's cave. Neurosurgery 41:7677751997

  • 36

    Samii MTatagiba MCarvalho GA: Retrosigmoid intradural suprameatal approach to Meckel's cave and the middle fossa: surgical technique and outcome. J Neurosurg 92:2352412000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Sanan AAbdel Aziz KMJanjua RMvan Loveren HRKeller JT: Colored silicone injection for use in neurosurgical dissections: anatomic technical note. Neurosurgery 45:126712741999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Seoane ERhoton AL Jr: Suprameatal extension of the retrosigmoid approach: microsurgical anatomy. Neurosurgery 44:5535601999

  • 39

    Stippler MGardner PASnyderman CHCarrau RLPrevedello DMKassam AB: Endoscopic endonasal approach for clival chordomas. Neurosurgery 64:2682782009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Taha JMTew JM Jrvan Loveren HRKeller JTel-Kalliny M: Comparison of conventional and skull base surgical approaches for the excision of trigeminal neurinomas. J Neurosurg 82:7197251995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Verstappen CCBeems TErasmus CEvan Lindert EJ: Dumbbell trigeminal schwannoma in a child: complete removal by a one-stage pterional surgical approach. Childs Nerv Syst 21:100810112005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42

    Yasuda ACampero AMartins CRhoton AL Jrde Oliveira ERibas GC: Microsurgical anatomy and approaches to the cavernous sinus. Neurosurgery 62:6 Suppl 3124012632008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Yuh WTWright DCBarloon TJSchultz DHSato YCervantes CA: MR imaging of primary tumors of trigeminal nerve and Meckel's cave. AJR Am J Roentgenol 151:5775821988

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Zhu JJPadillo ODuff JHsi BLFletcher JAQuerfurth H: Cavernous sinus and leptomeningeal metastases arising from a squamous cell carcinoma of the face: case report. Neurosurgery 54:4924992004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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Article Information

Contributor Notes

Correspondence Daniel M. Prevedello, Department of Neurosurgery, Wexner Medical Center at The Ohio State University, N-1049 Doan Hall, 410 West 10th Ave., Columbus, OH 43210. email: daniel.prevedello@osumc.edu.INCLUDE WHEN CITING Published online February 24, 2017; DOI: 10.3171/2016.10.JNS16381.Disclosures The authors report no conflict of interest concerning the materials and methods used in this study or the findings specified in this paper.
Headings
Figures
  • View in gallery

    EEA with a 0° endoscope (A, B, and C) and 30° endoscope (D, E, and F) showing the stepwise cadaveric dissection of the pterygopalatine fossa and cavernous sinus. A: Essential landmarks in an endoscopic endonasal skull base surgery are identified. This dissection was performed through a wide antrostomy exposing the posterior wall of the maxillary sinus; behind the bone it is possible to visualize the right infraorbital artery and its corresponding nerve going upward toward the right orbit. Superiorly and posteriorly, the lamina papyracea can be identified. Medially and superiorly to the lamina papyracea, located in the midline, is the cribriform plate, a critical structure in the surgical dissection to reach the anterior fossa. Inferiorly and posteriorly to the cribriform plate, also in the midline, 2 essential landmarks can be visualized: the sella and the clivus. B: Using a ball probe, we performed a dissection between the mucosa and the bone to expose the sphenopalatine foramen; this is a key landmark to identify since it contains the nasoseptal artery that provides blood supply to the nasoseptal flap, which has revolutionized endoscopic endonasal skull base surgery. Inferiorly and medially to the sphenopalatine foramen, the eustachian tube is located. C: A closer view of the sphenopalatine foramen and infraorbital nerve and its corresponding artery in the posterior wall of the maxillary sinus. D: The bone from the posterior wall of the maxillary sinus was removed to give access to the pterygopalatine fossa. The first identifiable layer is the periosteum. E: The bone and periosteum were removed to visualize some branches of the maxillary artery located in the pterygopalatine fossa. Lateral to the pterygopalatine fossa is the infratemporal fossa. The major terminal branch of the external carotid arteries is the maxillary artery that will give several branches; the most important one for skull base surgeons is the sphenopalatine artery. Other branches that can be visualized are the descending palatine artery and the posterior superior alveolar artery. Lateral to these structures is the temporal muscle in the infratemporal fossa. In the first plane it is possible to identify the arteries and the nerves behind it. In this figure panel we can also see the infraorbital nerve, which is an extension of the maxillary nerve after it crosses the foramen rotundum. F: The last step in the dissection of the lateral wall of the cavernous sinus and the QS. The vidian nerve was dissected in its entire pathway, starting from the pterygopalatine ganglion, which was removed, and ending in the foramen lacerum. On the lateral wall of the cavernous sinus are cranial nerve (CN) III, CNV1, CNV2, and the entire course of CNVI. The ICA was exposed from the foramen lacerum to the intracranial segment; therefore, after this dissection we can observe all the structures that compose the QS borders. AM = anteromedial; CNIII = oculomotor nerve; CNV1 = ophthalmic nerve; CNV2 = maxillary nerve; CNV3 = mandibular nerve; CNVI = abducens nerve; CP = cribriform plate; DPA = descending palatine artery; ET = eustachian tube; FR = foramen rotundum; Imax = internal maxillary artery; IOA = infraorbital artery; ION = infraorbital nerve; LP = lamina papyracea; pcICA = paraclival segment of ICA; PP = pterygoid process; PS = planum sphenoidale; PSAA = posterior superior alveolar artery; psICA = parasellar segment of ICA; PwMS = posterior wall of maxillary sinus; SPA = sphenopalatine artery; SPF = sphenopalatine foramen; TM = temporal muscle; VN = vidian nerve.

  • View in gallery

    Detailed 0° (A, B, and F) and 30° (C, D, and E) endoscopic views of the QS and surrounding structures. A: The bone on the right and left side of the lateral wall of the sphenoid sinus was removed. The dura was removed on the right side, allowing visualization of CNVI and the paraclival and parasellar segments of the ICA. On the left side, the dura was kept intact, and the lateral opticocarotid recess is visible superiorly; this is a critical landmark to recognize between the optic nerve and ICA; inferiorly, from lateral to medial, it is visualized by the impression of the maxillary strut and the maxillary nerve behind the dura. The portion of bone that was preserved in front of the QS, working like a shield to protect it, we named the “QS strut.” B: The QS strut was removed. C: With a 30° endoscope, the entire course of the vidian nerve can be seen along the vidian canal. It is possible to visualize the lateral recess of the sphenoid sinus, a space between the vidian nerve and the maxillary nerve. The dura around the lateral opticocarotid recess was removed to show the relationship between the parasellar segment of the ICA and the optic nerve. D: With the 30° endoscope, more details of the impression of the QS strut in the dura are visible. E: The dura around the paraclival segment of the ICA was removed, allowing a closer view of the vidian canal, lateral recess of the sphenoid sinus, and the impression of the maxillary nerve. F: The area around the QS in more detail; the sympathetic nerve fibers running with the paraclival segment of the ICA are visible, leaving it to join to the abducens nerve. CNII = optic nerve; iMS = impression of maxillary strut; iQSS = impression of QS strut; LOCR = lateral opticocarotid recess; LRSS = lateral recess of sphenoid sinus; QSS = QS strut; SF = sympathetic fibers; SS = sphenoid sinus; TS = tuberculum sellae; VC = vidian canal.

  • View in gallery

    Illustrations and anatomical dissection demonstrating the different ICA angles, their relation with the QS, and our proposed QS classification scheme. A: Illustration depicting a ventral perspective of an EEA. On the left, note the shadow of the right sphenoid bone and its corresponding superior orbital fissure and nerves; the nerves passing through the superior orbital fissure from superior to inferior are (in order) the lacrimal nerve, frontal nerve (a branch of the ophthalmic nerve), trochlear nerve (CNIV), superior division of the oculomotor nerve (CNIII), nasociliary nerve (a branch of the ophthalmic nerve), inferior division of the oculomotor nerve (CNIII), and the abducens nerve (CNVI). Superior to the superior orbital fissure, it is possible to identify the optic nerve and ophthalmic artery entering the optic canal. In addition, several anatomical structures and their relations are illustrated (superior to inferior); the optic chiasm is located superiorly, and lateral to it is CNII. Inferior to the chiasm is the pituitary stalk, which connects to the hypophysis. In the background, inferior to the pituitary gland, the vertebral arteries join themselves to form the basilar artery. The petrous, paraclival, parasellar, paraclinoid, and intradural segments of the left ICA are exposed. Lateral to the left ICA (superior to inferior) are CNII, CNIII, CNIV, CNV1, CNVI, CNV2, and CNV3. The QS is highlighted in blue. This is an area limited medially by the paraclival ICA, inferiorly by the horizontal petrous ICA, laterally by CNV2, and superiorly and obliquely by CNVI. B: Illustrations depicting the different types of ICA angle measurements on the right ICA. This classification scheme, proposed by Cebula et al., 2014, categorizes the angle between the parasellar and paraclival ICA segments into 1 of 4 types: < 80° (Type I), 80°–100° (Type II), > 100° (Type III), and asymmetrical (Type IV). The intercarotid space classification is highlighted in green. The intercarotid space is located between the parasellar and paraclival segments of both ICAs and is categorized based on its shape. The trapezoid shape is created when the course of the parasellar to paraclival segments of the ICA runs medial to lateral. With this type of intercarotid space, the distance between the ICAs in this trajectory (superior to inferior) widens. The square shape is created when the course of the parasellar to paraclival segments of the ICA is straight. The distance between the ICAs in this trajectory (superior to inferior) remains the same. The hourglass shape is created when the course of the parasellar to paraclival segments of the ICA is lateral to medial. The distance between the ICAs in this trajectory (superior to inferior) narrows. Our proposed QS classification is highlighted in blue. The QS is considered to be Type A when the shape of the intercarotid space (green) is trapezoid; the area and shape of the QS becomes narrower and shorter. The QS is considered to be Type B when the shape of the intercarotid space is square; the shape and area of the QS does not significantly alter. The QS is considered to be Type C when the intercarotid space has an hourglass shape; the area and shape of the QS becomes wider and longer. Images of cadaveric dissection of the left ICA, performed through an EEA using a 0° endoscope, mimic the illustrations. CNIV = trochlear nerve. Illustrations by Anthony Baker. Copyright The Ohio State University. Published with permission.

  • View in gallery

    Illustration depicting the distribution of ICA angle types in 44 cadaveric specimens (88 sides). The classification scheme developed by Cebula et al., based on the angle between the paraclival and parasellar segments of the ICA, was used. Twelve cadaveric specimens (27%) displayed a Type I angle, in which the angle between the paraclival and parasellar segments of the ICA is < 80° bilaterally. Three specimens (7%) displayed a Type II angle, in which the angle between the paraclival and parasellar segments of the ICA is 80°–100° bilaterally. Twenty specimens (46%) displayed a Type III angle, in which the angle between the paraclival and parasellar segments of the ICA is > 100° bilaterally. Nine specimens (20%) displayed a Type IV angle, in which the angle between the paraclival and parasellar segments of the ICA has a different type on each side.

  • View in gallery

    Graph depicting the relationship between ICA angle type and shape of the intercarotid space. A Type I angle (< 80°) was most commonly found in the 15 cadaveric specimens (34%) with a trapezoid-shaped intercarotid space. A Type III angle (> 100°) was most frequently found in the 16 cadaveric specimens (36%) with a square (straight)–shaped intercarotid space. A Type III angle (> 100°) was most commonly found in 13 cadaveric specimens (30%) with an hourglass-shaped intercarotid space. No Type I angles were observed with this conformation.

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    • PubMed
    • Search Google Scholar
    • Export Citation
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    Herzallah IRCasiano RR: Endoscopic endonasal study of the internal carotid artery course and variations. Am J Rhinol 21:2622702007

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    Inoue TRhoton AL JrTheele DBarry ME: Surgical approaches to the cavernous sinus: a microsurgical study. Neurosurgery 26:9039321990

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    Kassam ALabib MAPrevedello DMCarrau R: In reply: An endoscopic roadmap of the internal carotid artery. Neurosurgery 77:E154E1552015. (Letter)

    • Search Google Scholar
    • Export Citation
  • 23

    Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part I. Crista galli to the sella turcica. Neurosurg Focus 19:1E32005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part II. Posterior clinoids to the foramen magnum. Neurosurg Focus 19:1E42005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Kassam ABPrevedello DMCarrau RLSnyderman CHGardner POsawa S: The front door to Meckel's cave: an anteromedial corridor via expanded endoscopic endonasal approach—technical considerations and clinical series. Neurosurgery 64:3 Supplons71ons832009

    • Search Google Scholar
    • Export Citation
  • 26

    Kassam ABPrevedello DMCarrau RLSnyderman CHThomas AGardner P: Endoscopic endonasal skull base surgery: analysis of complications in the authors' initial 800 patients. J Neurosurg 114:154415682011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Kouyialis ATStranjalis GPapadogiorgakis NPapavlassopoulos FZiaka DSPetsinis V: Giant dumbbell-shaped middle cranial fossa trigeminal schwannoma with extension to the infratemporal and posterior fossae. Acta Neurochir (Wien) 149:9599642007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Kurbanov AZimmer LATheodosopoulos PVLeach JLKeller JT: An endoscopic roadmap of the internal carotid artery. Neurosurgery 77:E153E1542015. (Letter)

    • Search Google Scholar
    • Export Citation
  • 29

    Labib MAPrevedello DMCarrau RKerr EENaudy CAbou Al-Shaar H: A road map to the internal carotid artery in expanded endoscopic endonasal approaches to the ventral cranial base. Neurosurgery 10:Suppl 34484712014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Mascarenhas LMoshel YABayad FSzentirmai OSalek AALeng LZ: The transplanum transtuberculum approaches for suprasellar and sellar-suprasellar lesions: avoidance of cerebrospinal fluid leak and lessons learned. World Neurosurg 82:1861952014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Prevedello DMDitzel Filho LFSolari DCarrau RLKassam AB: Expanded endonasal approaches to middle cranial fossa and posterior fossa tumors. Neurosurg Clin N Am 21:621635vi2010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Prevedello DMDoglietto FJane JA JrJagannathan JHan JLaws ER Jr: History of endoscopic skull base surgery: its evolution and current reality. J Neurosurg 107:2062132007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Rhoton AL Jr: The cavernous sinus, the cavernous venous plexus, and the carotid collar. Neurosurgery 51:4 SupplS375S4102002

  • 34

    Rhoton AL Jr: The supratentorial arteries. Neurosurgery 51:4 SupplS53S1202002

  • 35

    Samii MCarvalho GATatagiba MMatthies C: Surgical management of meningiomas originating in Meckel's cave. Neurosurgery 41:7677751997

  • 36

    Samii MTatagiba MCarvalho GA: Retrosigmoid intradural suprameatal approach to Meckel's cave and the middle fossa: surgical technique and outcome. J Neurosurg 92:2352412000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Sanan AAbdel Aziz KMJanjua RMvan Loveren HRKeller JT: Colored silicone injection for use in neurosurgical dissections: anatomic technical note. Neurosurgery 45:126712741999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Seoane ERhoton AL Jr: Suprameatal extension of the retrosigmoid approach: microsurgical anatomy. Neurosurgery 44:5535601999

  • 39

    Stippler MGardner PASnyderman CHCarrau RLPrevedello DMKassam AB: Endoscopic endonasal approach for clival chordomas. Neurosurgery 64:2682782009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Taha JMTew JM Jrvan Loveren HRKeller JTel-Kalliny M: Comparison of conventional and skull base surgical approaches for the excision of trigeminal neurinomas. J Neurosurg 82:7197251995

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41

    Verstappen CCBeems TErasmus CEvan Lindert EJ: Dumbbell trigeminal schwannoma in a child: complete removal by a one-stage pterional surgical approach. Childs Nerv Syst 21:100810112005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42

    Yasuda ACampero AMartins CRhoton AL Jrde Oliveira ERibas GC: Microsurgical anatomy and approaches to the cavernous sinus. Neurosurgery 62:6 Suppl 3124012632008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Yuh WTWright DCBarloon TJSchultz DHSato YCervantes CA: MR imaging of primary tumors of trigeminal nerve and Meckel's cave. AJR Am J Roentgenol 151:5775821988

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Zhu JJPadillo ODuff JHsi BLFletcher JAQuerfurth H: Cavernous sinus and leptomeningeal metastases arising from a squamous cell carcinoma of the face: case report. Neurosurgery 54:4924992004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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