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The interperiosteodural concept applied to the jugular foramen and its compartmentalization

Florian Bernard, Ilyess Zemmoura, Jean Philippe Cottier, Henri-Dominique Fournier, Louis-Marie Terrier, and Stéphane Velut

OBJECTIVE

The dura mater is made of 2 layers: the endosteal layer (outer layer), which is firmly attached to the bone, and the meningeal layer (inner layer), which directly covers the brain and spinal cord. These 2 dural layers join together in most parts of the skull base and cranial convexity, and separate into the orbital and perisellar compartments or into the spinal epidural space to form the extradural neural axis compartment (EDNAC). The EDNAC contains fat and/or venous blood. The aim of this dissection study was to anatomically verify the concept of the EDNAC by focusing on the dural layers surrounding the jugular foramen area.

METHODS

The authors injected 10 cadaveric heads (20 jugular foramina) with colored latex and fixed them in formalin. The brainstem and cerebellum of 7 specimens were cautiously removed to allow a superior approach to the jugular foramen. Special attention was paid to the meningeal architecture of the jugular foramen, the petrosal inferior sinus and its venous confluence with the sigmoid sinus, and the glossopharyngeal, vagus, and accessory nerves. The 3 remaining heads were bleached with a 20% hydrogen peroxide solution. This procedure produced softening of the bone without modifying the fixed soft tissues, thus permitting coronal and axial dissections.

RESULTS

The EDNAC of the jugular foramen was limited by the endosteal and meningeal layers and contained venous blood. These 2 dural layers joined together at the level of the petrous and occipital bones and separated at the inferior petrosal sinus and the sigmoid sinus, and around the lower cranial nerves, to form the EDNAC. Study of the dural sheaths allowed the authors to describe an original compartmentalization of the jugular foramen in 3 parts: 2 neural compartments—glossopharyngeal and vagal—and the interperiosteodural compartment.

CONCLUSIONS

In this dissection study, the existence of the EDNAC concept in the jugular foramen was demonstrated, leading to the proposal of a novel 3-part compartmentalization, challenging the classical 2-part compartmentalization, of the jugular foramen.

In Journal of Neurosurgery Volume 129: Issue 3 (Sep 2018)

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Anatomy and white matter connections of the orbitofrontal gyrus

Joshua D. Burks, Andrew K. Conner, Phillip A. Bonney, Chad A. Glenn, Cordell M. Baker, Lillian B. Boettcher, Robert G. Briggs, Daniel L. O’Donoghue, Dee H. Wu, and Michael E. Sughrue

OBJECTIVE

The orbitofrontal cortex (OFC) is understood to have a role in outcome evaluation and risk assessment and is commonly involved with infiltrative tumors. A detailed understanding of the exact location and nature of associated white matter tracts could significantly improve postoperative morbidity related to declining capacity. Through diffusion tensor imaging–based fiber tracking validated by gross anatomical dissection as ground truth, the authors have characterized these connections based on relationships to other well-known structures.

METHODS

Diffusion imaging from the Human Connectome Project for 10 healthy adult controls was used for tractography analysis. The OFC was evaluated as a whole based on connectivity with other regions. All OFC tracts were mapped in both hemispheres, and a lateralization index was calculated with resultant tract volumes. Ten postmortem dissections were then performed using a modified Klingler technique to demonstrate the location of major tracts.

RESULTS

The authors identified 3 major connections of the OFC: a bundle to the thalamus and anterior cingulate gyrus, passing inferior to the caudate and medial to the vertical fibers of the thalamic projections; a bundle to the brainstem, traveling lateral to the caudate and medial to the internal capsule; and radiations to the parietal and occipital lobes traveling with the inferior fronto-occipital fasciculus.

CONCLUSIONS

The OFC is an important center for processing visual, spatial, and emotional information. Subtle differences in executive functioning following surgery for frontal lobe tumors may be better understood in the context of the fiber-bundle anatomy highlighted by this study.

In Journal of Neurosurgery Volume 128: Issue 6 (Jun 2018)

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Cavernous sinus compartments from the endoscopic endonasal approach: anatomical considerations and surgical relevance to adenoma surgery

Juan C. Fernandez-Miranda, Nathan T. Zwagerman, Kumar Abhinav, Stefan Lieber, Eric W. Wang, Carl H. Snyderman, and Paul A. Gardner

OBJECTIVE

Tumors with cavernous sinus (CS) invasion represent a neurosurgical challenge. Increasing application of the endoscopic endonasal approach (EEA) requires a thorough understanding of the CS anatomy from an endonasal perspective. In this study, the authors aimed to develop a surgical anatomy–based classification of the CS and establish its utility for preoperative surgical planning and intraoperative guidance in adenoma surgery.

METHODS

Twenty-five colored silicon–injected human head specimens were used for endonasal and transcranial dissections of the CS. Pre- and postoperative MRI studies of 98 patients with pituitary adenoma with intraoperatively confirmed CS invasion were analyzed.

RESULTS

Four CS compartments are described based on their spatial relationship with the cavernous ICA: superior, posterior, inferior, and lateral. Each compartment has distinct boundaries and dural and neurovascular relationships: the superior compartment relates to the interclinoidal ligament and oculomotor nerve, the posterior compartment bears the gulfar segment of the abducens nerve and inferior hypophyseal artery, the inferior compartment contains the sympathetic nerve and distal cavernous abducens nerve, and the lateral compartment includes all cavernous cranial nerves and the inferolateral arterial trunk. Twenty-nine patients had a single compartment invaded, and 69 had multiple compartments involved. The most commonly invaded compartment was the superior (79 patients), followed by the posterior (n = 64), inferior (n = 45), and lateral (n = 23) compartments. Residual tumor rates by compartment were 79% in lateral, 17% in posterior, 14% in superior, and 11% in inferior.

CONCLUSIONS

The anatomy-based classification presented here complements current imaging-based classifications and may help to identify involved compartments both preoperatively and intraoperatively.

In Journal of Neurosurgery Volume 129: Issue 2 (Aug 2018)

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Endoscopic extradural supraorbital approach to the temporal pole and adjacent area: technical note

Fuminari Komatsu, Masaaki Imai, Hideaki Shigematsu, Rie Aoki, Shinri Oda, Masami Shimoda, and Mitsunori Matsumae

The authors’ initial experience with the endoscopic extradural supraorbital approach to the temporal pole and adjacent area is reported. Fully endoscopic surgery using the extradural space via a supraorbital keyhole was performed for tumors in or around the temporal pole, including temporal pole cavernous angioma, sphenoid ridge meningioma, and cavernous sinus pituitary adenoma, mainly using 4-mm, 0° and 30° endoscopes and single-shaft instruments. After making a supraorbital keyhole, a 4-mm, 30° endoscope was advanced into the extradural space of the anterior cranial fossa during lifting of the dura mater. Following identification of the sphenoid ridge, orbital roof, and anterior clinoid process, the bone lateral to the orbital roof was drilled off until the dura mater of the anterior aspect of the temporal lobe was exposed. The dura mater of the temporal lobe was incised and opened, exposing the temporal pole under a 4-mm, 0° endoscope. Tumors in or around the temporal pole were safely removed under a superb view through the extradural corridor. The endoscopic extradural supraorbital approach was technically feasible and safe. The anterior trajectory to the temporal pole using the extradural space under endoscopy provided excellent visibility, allowing minimally invasive surgery. Further surgical experience and development of specialized instruments would promote this approach as an alternative surgical option.

In Journal of Neurosurgery Volume 128: Issue 6 (Jun 2018)

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Expanding the endoscopic transpterygoid corridor to the petroclival region: anatomical study and volumetric comparative analysis

Jacob L. Freeman, Raghuram Sampath, Steven Craig Quattlebaum, Michael A. Casey, Zach A. Folzenlogen, Vijay R. Ramakrishnan, and A. Samy Youssef

OBJECTIVE

The endoscopic endonasal transmaxillary transpterygoid (TMTP) approach has been the gateway for lateral skull base exposure. Removal of the cartilaginous eustachian tube (ET) and lateral mobilization of the internal carotid artery (ICA) are technically demanding adjunctive steps that are used to access the petroclival region. The gained expansion of the deep working corridor provided by these maneuvers has yet to be quantified.

METHODS

The TMTP approach with cartilaginous ET removal and ICA mobilization was performed in 5 adult cadaveric heads (10 sides). Accessible portions of the petrous apex were drilled during the following 3 stages: 1) before ET removal, 2) after ET removal but before ICA mobilization, and 3) after ET removal and ICA repositioning. Resection volumes were calculated using 3D reconstructions generated from thin-slice CT scans obtained before and after each step of the dissection.

RESULTS

The average petrous temporal bone resection volumes at each stage were 0.21 cm3, 0.71 cm3, and 1.32 cm3 (p < 0.05, paired t-test). Without ET removal, inferior and superior access to the petrous apex was limited. Furthermore, without ICA mobilization, drilling was confined to the inferior two-thirds of the petrous apex. After mobilization, the resection was extended superiorly through the upper extent of the petrous apex.

CONCLUSIONS

The transpterygoid corridor to the petroclival region is maximally expanded by the resection of the cartilaginous ET and mobilization of the paraclival ICA. These added maneuvers expanded the deep window almost 6 times and provided more lateral access to the petroclival region with a maximum volume of 1.5 cm3. This may result in the ability to resect small-to-moderate sized intradural petroclival lesions up to that volume. Larger lesions may better be approached through an open transcranial approach.

In Journal of Neurosurgery Volume 128: Issue 6 (Jun 2018)

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The suboccipital ligament

Kelsey Alabaster, M. Fred Bugg, Bruno Splavski, Frederick A. Boop, and Kenan I. Arnautovic

OBJECTIVE

A fibrous structure located dorsal to the dura at the posterior craniocervical junction stretches horizontally between the bilateral occipital condyles and the upper borders of the C-1 laminae. Partially covered by the occipital bone, this structure is always encountered when the bone is removed from the foramen magnum rim during approaches to the posterior cranial fossa. Although known to surgeons, this structure has not been defined, studied, or named. The most appropriate name for this structure is “the suboccipital ligament,” and a detailed rationale for this name is provided.

METHODS

This 3-year-long study included 10 cadaveric specimens and 39 clinical patients: 31 consecutive surgically treated patients with Chiari Type I malformations (CM-I subgroup) and 8 other patients with posterior fossa pathologies (non–CM-I subgroup). The dimensions were defined, the function of this ligament was hypothesized, size and histological composition were compared between patient subgroups, and its origin and relationship to the surrounding structures were analyzed. Possible statistical differences in the parameters between the 2 groups were also evaluated.

RESULTS

The suboccipital ligament consists of horizontally oriented hyaline fibers and has a median length of 35 mm, height of 10 mm, and thickness of 0.5 mm. These dimensions are not significantly different between the CM-I and non–CM-I patients. The median age of the patients was 43 years, with CM-I patients being significantly younger (median 35 years) than non–CM-I patients (median 57 years). There was no statistically significant difference in weight, height, and body mass index between patient subgroups. There was no significant correlation between the body mass index or height of the patients and the dimensions of the ligament. No statistically significant differences existed between the subgroups in terms of smoking history, alcohol consumption, and the presence of diabetes mellitus, hypertension, hydrocephalus, or headaches. The ligament tissue in the CM-I patients was disorganized with poorly arranged collagen bands and interspersed adipose tissue. These patients also had more hyalinized fibrosis and showed changes in the direction of fibers, with hyaline nodules ranging from 0 to 2+. The result of the histological evaluation of the suboccipital ligament for hyaline nodules, calcification, and ossification was graded as 2+ if present in 3 or more medium-power magnification fields (MPFs); 1+ if present in 1–2 MPFs; and 0, if present in less than 1 MPF. Histological examination of the ligaments showed structural differences between CM-I and non–CM-I patients, most notably the presence of hyaline nodules and an altered fiber orientation in CM-I patients.

CONCLUSIONS

The suboccipital ligament extends between the occipital condyle and the superior edge of the C-1 lamina, connecting the contralateral sides, and appears to function as a real ligament. It is ventral to the occipital bone, which covers approximately two-thirds of the height of the ligament and is loosely attached to the dura medially and more firmly laterally. Because of its distinctive anatomy, characteristics, and function, the suboccipital ligament deserves its own uniform designation and name.

In Journal of Neurosurgery Volume 128: Issue 1 (Jan 2018)

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The interpeduncular fossa approach for resection of ventromedial midbrain lesions

M. Yashar S. Kalani, Kaan Yağmurlu, and Robert F. Spetzler

The authors describe the interpeduncular fossa safe entry zone as a route for resection of ventromedial midbrain lesions. To illustrate the utility of this novel safe entry zone, the authors provide clinical data from 2 patients who underwent contralateral orbitozygomatic transinterpeduncular fossa approaches to deep cavernous malformations located medial to the oculomotor nerve (cranial nerve [CN] III). These cases are supplemented by anatomical information from 6 formalin-fixed adult human brainstems and 4 silicone-injected adult human cadaveric heads on which the fiber dissection technique was used.

The interpeduncular fossa may be incised to resect anteriorly located lesions that are medial to the oculomotor nerve and can serve as an alternative to the anterior mesencephalic safe entry zone (i.e., perioculomotor safe entry zone) for resection of ventromedial midbrain lesions. The interpeduncular fossa safe entry zone is best approached using a modified orbitozygomatic craniotomy and uses the space between the mammillary bodies and the top of the basilar artery to gain access to ventromedial lesions located in the ventral mesencephalon and medial to the oculomotor nerve.

In Journal of Neurosurgery Volume 128: Issue 3 (Mar 2018)

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The white matter tracts of the cerebrum in ventricular surgery and hydrocephalus

Abuzer Güngör, Serhat Baydin, Erik H. Middlebrooks, Necmettin Tanriover, Cihan Isler, and Albert L. Rhoton Jr.

OBJECTIVE

The relationship of the white matter tracts to the lateral ventricles is important when planning surgical approaches to the ventricles and in understanding the symptoms of hydrocephalus. The authors' aim was to explore the relationship of the white matter tracts of the cerebrum to the lateral ventricles using fiber dissection technique and MR tractography and to discuss these findings in relation to approaches to ventricular lesions.

METHODS

Forty adult human formalin-fixed cadaveric hemispheres (20 brains) and 3 whole heads were examined using fiber dissection technique. The dissections were performed from lateral to medial, medial to lateral, superior to inferior, and inferior to superior. MR tractography showing the lateral ventricles aided in the understanding of the 3D relationships of the white matter tracts with the lateral ventricles.

RESULTS

The relationship between the lateral ventricles and the superior longitudinal I, II, and III, arcuate, vertical occipital, middle longitudinal, inferior longitudinal, inferior frontooccipital, uncinate, sledge runner, and lingular amygdaloidal fasciculi; and the anterior commissure fibers, optic radiations, internal capsule, corona radiata, thalamic radiations, cingulum, corpus callosum, fornix, caudate nucleus, thalamus, stria terminalis, and stria medullaris thalami were defined anatomically and radiologically. These fibers and structures have a consistent relationship to the lateral ventricles.

CONCLUSIONS

Knowledge of the relationship of the white matter tracts of the cerebrum to the lateral ventricles should aid in planning more accurate surgery for lesions within the lateral ventricles.

In Journal of Neurosurgery Volume 126 (2017): Issue 3 (Mar 2017)

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

Ricardo L. L. Dolci, Leo F. S. Ditzel Filho, Carlos R. Goulart, Smita Upadhyay, Lamia Buohliqah, Paulo R. Lazarini, Daniel M. Prevedello, and Ricardo L. Carrau

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.

In Journal of Neurosurgery Volume 128: Issue 1 (Jan 2018)

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The rectus capitis lateralis and the condylar triangle: important landmarks in posterior and lateral approaches to the jugular foramen

Michael A. Cohen, Alexander I. Evins, Gennaro Lapadula, Leopold Arko, Philip E. Stieg, and Antonio Bernardo

OBJECTIVE

The rectus capitis lateralis (RCL) is a small posterior cervical muscle that originates from the transverse process of C-1 and inserts onto the jugular process of the occipital bone. The authors describe the RCL and its anatomical relationships, and discuss its utility as a surgical landmark for safe exposure of the jugular foramen in extended or combined skull base approaches. In addition, the condylar triangle is defined as a landmark for localizing the vertebral artery (VA) and occipital condyle.

METHODS

Four cadaveric heads (8 sides) were used to perform far-lateral, extended far-lateral, combined transmastoid infralabyrinthine transcervical, and combined far-lateral transmastoid infralabyrinthine transcervical approaches to the jugular foramen. On each side, the RCL was dissected, and its musculoskeletal, vascular, and neural relationships were examined.

RESULTS

The RCL lies directly posterior to the internal jugular vein—only separated by the carotid sheath and in some cases cranial nerve (CN) XI. The occipital artery travels between the RCL and the posterior belly of the digastric muscle, and the VA passes medially to the RCL as it exits the C-1 foramen transversarium and courses posteriorly toward its dural entrance. CNs IX–XI exit the jugular foramen directly anterior to the RCL. To provide a landmark for identification of the occipital condyle and the extradural VA without exposure of the suboccipital triangle, the authors propose and define a condylar triangle that is formed by the RCL anteriorly, the superior oblique posteriorly, and the occipital bone superiorly.

CONCLUSIONS

The RCL is an important surgical landmark that allows for early identification of the critical neurovascular structures when approaching the jugular foramen, especially in the presence of anatomically displacing tumors. The condylar triangle is a novel and useful landmark for identifying the terminal segment of the hypoglossal canal as well as the superior aspect of the VA at its exit from the C-1 foramen transversarium, without performing a far-lateral exposure.

In Journal of Neurosurgery Volume 127: Issue 6 (Dec 2017)