ABBREVIATIONS:
CCA
carotid arteries
CS
cavernous sinus
FR
foramen rotundum
IJV
internal jugular veins
SOF
superior orbital fissure
TONES
transorbital neuroendoscopic surgeryVN
Vidian nerve
VELPPHA
Vidian nerve, Eustachian tube, foramen lacerum, petroclival fissure, and pharyngobasilar fascia.
The cavernous sinus (CS) is a complex venous sinus at the inner part of the skull base. It extends from the superior orbital fissure (SOF) following the interclinoid ligament up to the posterior clinoid medially and the trigeminal pore laterally on its superior limit and from the foramen rotundum (FR) following the second trigeminal nerve (V2) up to the petroclival fissure on its inferior limit. Anteriorly, it follows the anterior margin of the SOF up to the FR, whereas posteriorly, it goes from the dorsum sellae to the petroclival fissure and communicates with the basilar plexus medially and with superior and inferior petrosal sinus laterally. Medially is limited by the sphenoid sinus and the pituitary gland, whereas laterally is limited by the dura mater of the mesial temporal lobe.1,2
Classically, the CS was divided by Harris and Rhoton into medial, anteroinferior, posterosuperior, and lateral compartments from a transcranial anatomic point of view. The medial compartment is between the pituitary gland and the internal carotid artery (ICA), the anteroinferior compartment is located below the first curve of the internal carotid artery, the posterosuperior compartment is from the posterior half of the roof of the sinus to the carotid, and the lateral compartment is located between the lateral sinus wall and the ICA.1,3
At the beginning of the 20th century, first approaches to the sphenoid sinus and adjacent CS areas were performed through microscopic endonasal approaches such as the sublabial, transseptal, and transsphenoidal approaches standardized by Cushing and popularized by Guiot and Hardy.3,4 4-6
Several transcranial routes are reported in the literature to reach the CS, the pterional craniotomy described in 1976 by Yasargil7,8 9-12 13 14 15 16
Recently, a new transorbital endoscopic approach throughout the superior eyelid to reach the CS area was described by Kris Moe.17 18-27
The anatomic comparison between the transcranial and endonasal endoscopic approaches to the CS is well exposed in the literature.25-31
METHODS
Anatomic Dissections
For the dissection, 6 sides from 3 cadaveric heads were used for the anatomic dissections at the Laboratory of Surgical Neuroanatomy of the Human Anatomy and Embryology Unit, University of Barcelona (Barcelona, Spain). Using the Cambridge technique, each head was fixed through the canalization of common carotid arteries (CCA) and internal jugular veins (IJV). After fixation, red latex and blue latex were injected through CCA and IJV, respectively.
To adequately visualize the CS, MRI T2 and T1 sequences were performed in one of the heads. Later, 6 screws were implanted at the cranial vault of each specimen as reference markers to allow navigation with manual point registration in our neuronavigation system (Medtronic, Inc. Surgical Technologies). Multislice helical computed tomography scan (Siemens SOMATOM Sensation 64) with 0.6-mm-thick axial spiral sections and a 0° gantry angle was performed in all heads before and after the dissection of each approach.
Before dissection, MRI and CT scan imaging data were transferred to the laboratory navigation planning workstation, and registration was performed, as previously mentioned by our group.28-30
For the microscopic dissection of the transcranial and initial steps of the transorbital approach, a Zeiss OPMIR® microscope was used with magnifications ranging from ×3 to ×40, whereas for the endoscopic dissection of endonasal and transorbital approaches, a rigid endoscope 4 mm in diameter and 18 cm in length, with a 0° lens (Karl Storz) was used. In both cases, the endoscope and microscope were connected to a high-definition camera (Endovision Telecam SL; Karl Storz) for image and video recording.
Then, cadaveric dissections were performed as follows.
Endoscopic Endonasal Approach
A lateral extended transpterygoid approach was performed as proposed by Kassam et al6 31 1 .
FIGURE 1.: Endoscopic endonasal transpterygoid approach. Notice the bony bulges of V2 (V2), maxillary strut (Max. Strut), the superior orbital fissure (Sup. Orb. Fissure), the medial opticocarotid recess (Med. Opticocar. Rec.), the lateral opticocarotid recess (Lat. Opticocar. Rec.), the internal carotid artery (Int. Car. Artery), and the clivus. Also visible are the pituitary gland and the inferior intercavernous sinus (Inf. Intercav. Sinus). On the right side of the image, the bone is removed, exposing the left cavernous sinus.
Superior Eyelid Endoscopic Transorbital Approach
As first described by Kris Moe17 19,22,30,32 transorbital neuroendoscopic surgery (TONES) approach was made through a superior eyelid incision. Subperiosteal dissection was performed within the orbit until the inferior and SOF were identified, and the bone between them was removed, exposing the temporal muscle and the temporal dura. Bone drilling was continued at the level of the middle cranial fossa until the identification of the FR. At this level, the meningo-orbital band could be identified and cut to access the CS.33 2 .
FIGURE 2.: Right side transorbital endoscopic approach exposing the lateral wall of the cavernous sinus peeled. The ophthalmic nerve (V1) exiting the superior orbital fissure, the maxillary nerve (V2) exiting the foramen rotundum, and the mandibular nerve (V3) exiting through the foramen ovale; III nerve (III), IV nerve (IV), the Gasserian ganglion and the trigeminal pore (trig. Pore), infratrochlear triangle (infratroc. Triangle), anteromedial triangle (Ant. Med Triangle), posterior clinoid process (Post. Clin. Pr.), and the middle meningeal artery (Mid. Men. Art.) going out the foramen spinosum.
Transcranial Approach—Pterional Approach
Pterional craniotomy with extradural clinoidectomy was performed as described in the literature.9,12,34-36 3 .
FIGURE 3.: Right transcranial approach exposing the lateral and superior cavernous sinus peeled. The anterior petroclinoid fold partially hides the III nerve (III) (*), IV nerve (IV), ophthalmic nerve (V1), maxillary nerve (V2), and the Gasserian ganglion; clinoidal triangle exposing the internal carotid artery (§) and part of the cavernous sinus. The dotted line represents the anterior clinoid removed.
Quantitative Analysis
The CS area exposed through each approach was calculated using the Brainlab cranial navigation system as previously described by this group.29,30,37 Table shows the anatomic landmarks used for each.
TABLE. -
Cavernous Sinus (CS) Landmark Limits Acquired for Quantitative Analysis
CVS landmark limits
Endonasal approach
Transorbital approachTranscranial approach
Anterosuperior (P1)
SOF (eP1)
SOF (toP1)
SOF (tP1)
Anteroinferior (P2)
FR (eP2)
FR (toP2)
FR (tP2)
Posterosuperior (P3)
Dorsum sellae (eP3)
Trigeminal pore (toP3)
Trigeminal pore (tP3)
Posteroinferior (P4)
IV nerve exiting Dorello's canal (eP4)
V2 prolongation into cisternal trigeminal ganglion (toP4)
V2 prolongation into cisternal trigeminal ganglion (tP4)
FR, Foramen rotundum; SOF, superior orbital fissure.
Points registered are expressed as cartesian coordinates (x,y,z) on the Brainlab workstation. Each point was acquired 3 times, the arithmetic mean for each coordinate was calculated, and 2 juxtaposed scalene triangles were generated. Thus, the total exposed area was calculated as the sum of both triangles.
Furthermore, a virtual 3-dimensional model of the exposed areas was created using Amira Visage Imaging software, acquiring multiple points all over the exposed CS surface and merged with the mentioned software.
RESULTS
Extradural CS exposure was performed in all specimens, and anatomic landmark identification was possible in all cases.
Qualitative Analysis
Endoscopic Endonasal Approach
The CS dura's medial side was exposed from V2 exiting the FR at its anteroinferior point up to the SOF at its anterosuperior end and back to the dorsum sellae and paraclinoid area.
The VI nerve traveling from Dorello's canal to the SOF was identified entering the CS. The most proximal intracavernous part of the nerve, the proximal portion of the V2 nerve, and the trigeminal ganglion were blocked by paraclival ICA and the carotid sympatico plexus. Visualization of this CS portion was achieved after medial retraction of the paraclival ICA and excessive manipulation of the sympathetic branches. The III and V2 nerves marked the superior and inferior limits of the sinus, respectively. In contrast to the V2 nerve, the III nerve is barely seen without medial retraction of the anterior bend of the ICA. The remaining posterosuperior part of the sinus was partially accessed, retracting the pituitary gland medially,38 4 .
FIGURE 4.: A , Exposed left cavernous sinus without the medial wall, filled with blue latex, and right CS without exposing the VI nerve (VI) and the maxillary nerve (V2). B , Access to the medial compartment after cutting the parasellar ligaments. C , Access to the inferior and posterior compartment displacing the internal carotid medially the IV, V2, and the sympathetic plexus. D , Access to the anterior part of the superior compartment displacing the carotid medially exposing the III nerve (III) and the VI.
Transorbital ApproachThe section of the meningo-orbital band allows the interdural CS dissection and exposure of the whole lateral side of the CS from the SOF and FR back to the cisternal part of the trigeminal ganglion and the dorsum sellae. The III, IV, V1, and V2 nerves were identified on the lateral wall of the CS and the V3 nerve going to the foramen ovale. Dissection was extended until the trigeminal pore and the petrous apex without significant dural retraction. The CS was accessed through the infratrochlear triangle.
Transcranial Pterional Approach
The resection of the anterior clinoid process allowed access to the clinoidal and oculomotor triangles at the superior side of the CS. Furthermore, exposure to the lateral CS wall was also possible with dural retraction. The III, IV, V1, and V2 nerves were exposed through this approach. Partial exposure to the CS was performed through the clinoidal, oculomotor, and infratrochlear triangles.
The VI nerve, medial compartment of the CS, and some parts of the cavernous ICA could not be seen through this approach without a pretemporal, subtemporal, or orbitozygomatic expansion.
Quantitative Analysis
The arithmetic means of the accessible CS areas and volumes reached throughout each approach are as follows:
1. Endoscopic endonasal approach: 215 mm2 and 1142 mm3 .
2. Transcranial pterional approach: 311 mm2 and 817 mm3 .
3. Transorbital approach: 372 mm2 and 750 mm3 .
The anatomic location of each area and volume is illustrated in Figures 5 -7 .
FIGURE 5.: Left transorbital approach. Left: anterior view of the lateral cavernous sinus (CS) with the III nerve (III), the IV nerve (IV), the ophthalmic nerve (V1), maxillary nerve (V2), and the mandibular nerve (V3) exiting the trigeminal ganglion. The anterior petroclinoid ligament limits the superior aspect. Right: posterior view of the lateral CS exposing the IV, V1, V2, and V3, all the trigeminal ganglion traveling to the trigeminal pore. The infratrochlear triangle is delimited by the IV and V1 nerves exposing the remaining blue latex of the CS. CS, cavernous sinus.
FIGURE 6.: Navigation points acquired as cavernous sinus limits on the superior images and calculated area for those points on the inferior images. A , 1, 2 Endoscopic endonasal approach. B , 1, 2. Transcranial pterional approach. C , 1, 2. Transorbital approach.
FIGURE 7.: Calculated volumes for the A , endoscopic endonasal approach, B , transcranial pterional approach; and C , transorbital approach. Combined calculated volumes from A , D , superior and E , anterior views.
DISCUSSION
In 2018, a new CS compartment classification was proposed by Fernandez-Miranda et al, subdividing the sinus according to its relation with the cavernous ICA. The area above the horizontal segment of the cavernous ICA is the superior compartment, whereas the area below is the inferior one. Similarly, the area behind the vertical segment of the cavernous ICA is the posterior compartment, whereas the area lateral to it is the lateral one. Regarding the medial compartment described by Harris and Rhoton,1,3 39
Despite similar CS areas and volumes calculated for each approach, remarkable differences were encountered between them when comparing the anatomic location of each one. Considering the Fernandez-Miranda CS classification, the endonasal approach allowed easy access to all the inferior and part of the superior CS compartments without ICA or nerve retraction. Meanwhile, the access to the lateral or posterior compartments required nerve and ICA retraction.
Conversely, the transorbital approach allowed a direct route to the lateral wall, accessing the V1, V2, and V3 nerves; the trigeminal ganglion back to the trigeminal porus; and the petrous apex, as previously mentioned in the literature.40,41 transorbital approach equals the subtemporal one to reach the mentioned middle fossa structures, the angles of attack and surgical freedom are significantly inferior in the transorbital approach and demand higher cadaver training because of the unfamiliar perspective.41
Arterial bleeding could be difficult to control through endoscopic approaches, and ICA cavernous branches must be considered when entering CS compartments. Despite anatomic variations, the most consistent branches are the inferior cavernous artery or lateral trunk arising from the horizontal segment of the ICA and the meningohypophyseal or posterior trunk emerging at the posterior bend of the ICA inside the posterior compartment of the CS.42,43
The dissection through the classical transcranial pterional approach allowed clear visualization of the superior wall of the CS and the clinoidal and oculomotor triangles as well as part of the lateral wall and the infratrochlear and anteromedial triangles, partially accessing the superior and lateral CS compartments, as mentioned in the previous literature.42
Tumors near the sellar and parasellar areas tend to invade CS compartments. Combined simultaneous approaches to these areas can achieve better tumor resection, as more frequently reported in the literature.44-48
Study Limitations
The main limitation of our study is the use of only 1 transcranial approach. Other commonly used approaches, such as the half-and-half, the pretemporal, the subtemporal, or the orbitozygomatic approaches, offer a better transcranial exposure of the lateral wall of the CS and even good access to all the sinus compartments as referred by Hakuba.13,14,16,49
Furthermore, our results are based on cadaveric dissection, which had significant anatomic variability interspecimen and differs considerably from clinical practice, where aggressive dissection could equal nerve palsy. Moreover, our quantitative analysis is based on a point registration from the neuronavigation plan, and the margin of error must be considered.
CONCLUSION
Based on the CS compartment classification and the obtained results, we observed that the endoscopic approach is the direct access to reach all the medial, inferior, and part of the superior CS compartments, the transorbital route for the lateral side and part of the superior and lateral CS compartment, and the classical transcranial pterional approach for the superior side of the CS and its superior compartment. Despite this, other transcranial routes not studied in this article can reach the lateral side and the posterior and inferior compartments of the sinus.
Funding
This study was funded by the Spanish Society of Neurological Surgeons (SENEC) and the Instituto de Salud Carlos III (ISCIII) through the project PI19/00592 and cofunded by the European Union and the “Fundació La Marató de TV3” (Reg. 95/210; Codi projecte 201914).
Disclosures
The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.
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COMMENTS
In this article, the authors report a brilliant perspective over 3 different surgical corridors to unlock the different areas of the cavernous sinus: aside from the peer anatomic description offered, it has presented a comparison with quantitative analysis of the possibilities of 2 solid corridors, ie, the pterional and the endoscopic endonasal vs the neuroendoscopic transorbital . The latter corridor has been recently given credit as a viable surgical approach to enter and manage safely middle fossa lesions, and the same group of authors has detailed anatomic landmarks and surgical hints of this route.
Together with other groups, we have promoted the development of endoscopic endonasal skull base surgery and we are proud to having lighted the “spark” for the innovation of transorbital window during a course in Naples, back in 2014.
It might be said that there is still skepticism in regard to the transorbital endoscopic approach among the scientific community, whereas the enthusiast acolytes of this idea praise its features as per the ascending slope of Scott's parabola.1a
The present anatomic study is a further step forward, and the results are utterly valuable for providing a useful quantitative esteem of the surgical maneuverability, therefore giving a real surgical perception of the transorbital approach to the cavernous sinus.
On one side, its concrete attitude of measuring in math the approaches fits the modern neurosurgery scenario, leant toward minimally invasiveness; on the other side, it embraces the concept of surrounding the disease from different angles, as per the so-called multiportal approach—combining approaches in 1 surgery or having a multistep procedure.
This is a beautiful story of translational medicine started from anatomic research and moved into the operating theater on living patients.
Luigi M. Cavallo
Domenico Solari
Paolo Cappabianca
Naples, Italy
References
1a. Cappabianca P, Doglietto F, Gentili F, Nicolai P. Endoscopic skull base surgery: where on the parabola? J Neurosurg Sci. 2016;60(4):438-440.
Unfortunately, this article perpetuates many inaccuracies regarding cavernous sinus surgery and presents conclusions that are purely academic and not transferable to surgical practice. The most apparent shortcoming of this article is the clearly insufficient application of transcranial surgical techniques for access to the cavernous sinus, invalidating the presented comparison between approaches. In surgery, a sufficient transcranial approach offers not only extradural access to the lateral, posterior, and anterior compartments after removal of the anterior clinoid—including the carotid cave—but also offers the intradural corridor through the roof of the cavernous sinus medially to the oculomotor nerve with excellent visualization of the medial component of the cavernous sinus, especially when invaded and enlarged by a tumor from the perisellar or sellar regions. A combined intra- and extradural transcranial route, when correctly performed, with preparatory techniques offers optimal visualization of the entire parasellar compartment that is clinically superior to the other approaches evaluated. The position of the superior orbital fissure, with its intra- and extra-annular components, greatly limits the cavernous sinus spaces through an anterior perspective, but unroofing of the superior orbital fissure in a transcranial approach and displacing the extra-annual structures, along with other surgical maneuvers, allow for the safe freeing of cranial nerves 3 and 4 and the subsequent safe opening of Parkinson's triangle. The extremely limited spaces of the transorbital approach together with the presence of venous blood do not make these surgical corridors comparable with the greater surgical maneuverability and exposure provided by traditional approaches. Furthermore, most lesions that invade the cavernous sinus originate from elsewhere, and the transorbital approach would thus only be applicable to hypothetical small lesions confined only to the cavernous sinus. Overall, the quantitative conclusions presented denote conspicuous inaccuracies dictated by an insufficient transcranial surgical technique. As such, the use of transcranial approaches herein is rather in name only, as no surgical maneuvers that would allow for access to the cavernous sinus were performed, rendering the transcranial approach as the ostensible straw man. Moreover, given that the conclusions are so inapplicable to clinical practice, the value of such publications must be questioned.
Antonio Bernardo
Alexander I. Evins
New York, New York, USA
