Fine configuration of the dural fibrous network and the extradural neural axis compartment in the jugular foramen: an epoxy sheet plastination and confocal microscopy study

Jacob D. Bond BSc(Hons)1,2, Zhaoyang Xu MB, MMed1, and Ming Zhang MB, MMed, PhD1,3
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  • 1 Department of Anatomy and
  • | 2 Dunedin School of Medicine, University of Otago, Dunedin, New Zealand; and
  • | 3 Department of Anatomy, Anhui Medical University, Hefei, China
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OBJECTIVE

The extradural neural axis compartment (EDNAC) is an adipovenous zone that is located between the meningeal (ML) and endosteal (EL) layers of the dura mater and has been minimally investigated in the jugular foramen (JF) region. In this study, the authors aimed to explore the fine architecture of the EDNAC within the JF and evaluate whether the EDNAC can be used as a component for JF compartmentalization.

METHODS

A total of 46 cadaveric heads (31 male, 15 female; age range 54–96 years) and 30 dry skulls were examined in this study. Twelve of 46 cadaveric heads were plastinated as a series of transverse (7 sets), coronal (3 sets), and sagittal (2 sets) slices and examined using stereomicroscopy and confocal microscopy. The dural entry points of the JF cranial nerves were recorded in 34 cadaveric skulls. The volumes of the JF, intraforaminal EDNAC, and internal jugular vein (IJV) were quantified.

RESULTS

Based on constant osseous landmarks, the JF was subdivided into preforaminal, intraforaminal, and subforaminal segments. The ML-derived fascial sheath along the anteromedial wall of the IJV demarcated the “venous portion” and the “EDNAC portion” of the bipartite JF. The EDNAC did not surround the intraforaminal IJV and comprised an ML-derived dural fibrous network and an adipose matrix. A fibrovenous curtain subdivided the intraforaminal EDNAC into a small anterior column containing cranial nerve (CN) IX and the anterior condylar venous plexus and a large posterior adipose column containing CNs X and XI. In the intraforaminal segment, the IJV occupied a slightly larger space in the foramen (57%; p < 0.01), whereas in the subforaminal segment it occupied a space of similar size to that of the EDNAC.

CONCLUSIONS

Excluding the IJV, the neurovascular structures in the JF traverse the dural fibrous network that is dominant in the foraminal EDNAC. The results of this study will contribute to anatomical knowledge of the obscure yet crucially important JF region, increase understanding of foraminal tumor growth and spread patterns, and facilitate the planning and execution of surgical interventions.

ABBREVIATIONS

ACV = anterior condylar vein; CN = cranial nerve; EDNAC = extradural neural axis compartment; EL = endosteal dural layer; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; JB = jugular bulb; JF = jugular foramen; ML = meningeal dural layer; RCL = rectus capitis lateralis; SS = sigmoid sinus.

OBJECTIVE

The extradural neural axis compartment (EDNAC) is an adipovenous zone that is located between the meningeal (ML) and endosteal (EL) layers of the dura mater and has been minimally investigated in the jugular foramen (JF) region. In this study, the authors aimed to explore the fine architecture of the EDNAC within the JF and evaluate whether the EDNAC can be used as a component for JF compartmentalization.

METHODS

A total of 46 cadaveric heads (31 male, 15 female; age range 54–96 years) and 30 dry skulls were examined in this study. Twelve of 46 cadaveric heads were plastinated as a series of transverse (7 sets), coronal (3 sets), and sagittal (2 sets) slices and examined using stereomicroscopy and confocal microscopy. The dural entry points of the JF cranial nerves were recorded in 34 cadaveric skulls. The volumes of the JF, intraforaminal EDNAC, and internal jugular vein (IJV) were quantified.

RESULTS

Based on constant osseous landmarks, the JF was subdivided into preforaminal, intraforaminal, and subforaminal segments. The ML-derived fascial sheath along the anteromedial wall of the IJV demarcated the “venous portion” and the “EDNAC portion” of the bipartite JF. The EDNAC did not surround the intraforaminal IJV and comprised an ML-derived dural fibrous network and an adipose matrix. A fibrovenous curtain subdivided the intraforaminal EDNAC into a small anterior column containing cranial nerve (CN) IX and the anterior condylar venous plexus and a large posterior adipose column containing CNs X and XI. In the intraforaminal segment, the IJV occupied a slightly larger space in the foramen (57%; p < 0.01), whereas in the subforaminal segment it occupied a space of similar size to that of the EDNAC.

CONCLUSIONS

Excluding the IJV, the neurovascular structures in the JF traverse the dural fibrous network that is dominant in the foraminal EDNAC. The results of this study will contribute to anatomical knowledge of the obscure yet crucially important JF region, increase understanding of foraminal tumor growth and spread patterns, and facilitate the planning and execution of surgical interventions.

ABBREVIATIONS

ACV = anterior condylar vein; CN = cranial nerve; EDNAC = extradural neural axis compartment; EL = endosteal dural layer; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; JB = jugular bulb; JF = jugular foramen; ML = meningeal dural layer; RCL = rectus capitis lateralis; SS = sigmoid sinus.

In Brief

The authors investigated the fine architecture of the fibrous network and fatty matrix in the jugular foramen. The resulting presentation of these anatomical details may aid neurosurgeons in planning surgical approaches to the region and increase understanding of how tumors in this area grow.

The extradural neural axis compartment (EDNAC) is an adipovenous space sandwiched between the outer endosteal dural layer (EL) and inner meningeal dural layer (ML) that extends from the orbit to the coccyx.1 The primary element of the EDNAC is fat, which frequently contains valveless veins and is often accompanied by traversing peripheral nerves and vascular structures.1–6 Movement of the eye, lubrication of the dural layers during flexion and extension of the spine, and cushioning and support of traversing nerves and vessels are all conjectured functions of the EDNAC.7–9 Understanding the configuration of the EDNAC within the JF may provide a means to predict the growth pattern of tumors in this area and might help inform operative approaches.

Recently, Bernard et al. (2018) demonstrated that the EDNAC exists in the jugular foramen (JF), and that cranial nerves (CNs) IX–XI and their dural sheaths and the distal sigmoid sinus (SS) and inferior petrosal sinus (IPS) course within the foraminal EDNAC.6 Liang et al. (2019) also depicted a venous plexus within the JF suspended in an adipose matrix.10 The EDNAC presence within the foramen was even designated as a foraminal compartment by Bernard et al.6 Compartmentalization of the JF is controversial due to its irregular morphology and the complexity of its crowded contents; indeed, 4 different compartmental models have been proposed so far.11

At present, there is a dearth of literature concerning the EDNAC, let alone its presence within the JF.6 It has been reported that within the parasellar EDNAC compartment the traversing neurovascular structures are supported by both an adipose matrix and a dural fibrous network. This dural network originates from the ML and continues with neurovascular sheaths and the adipose matrix to form a skeleton of fibrous struts within the EDNAC.12 Bernard et al. dissected the dural layers surrounding the JF area and defined the dural fibrous thickenings anterior and posterior to CN IX as an “intrajugular ligament.”6 The intrajugular ligament separates CN IX from CNs X and XI and serves as a surgical border to protect the lower cranial nerves. However, Bernard et al. noted that it was impossible to ascertain the origin and configuration of this intraforaminal ligament from a macroscopic perspective.6 Therefore, in the present study we aimed to explore the configuration and distribution of the EDNAC, particularly its dural fibrous network component, within the JF, and in doing so test whether the EDNAC can be used as a practical element for JF compartmentation.

Methods

In this study we examined a total of 46 cadaveric heads (31 male, 15 female; age range 54–96 years; 12 for plastination and 34 for dural entry mapping) and 30 dry skulls. The human material used in this investigation was all sourced, studied, and stored in accordance with the Human Tissue Act (New Zealand, 2008). Ethical approval for this study was obtained from the University of Otago Human Ethics Committee (Health), in conjunction with Māori consultation being sought from the Ngāi Tahu Research Consultation Committee.

Plastination

Twelve cadavers (7 male, 5 female; age range 54–87 years) were plastinated as a series of transverse (7 sets), coronal (3 sets), and sagittal (2 sets) slices. The plastination procedure replaces the water and fat content of tissues with epoxy resin, resulting in durable, transparent slices that can be observed from both macroscopic and microscopic perspectives and allow study in situ of the preserved anatomy of delicate structures that might otherwise be damaged or destroyed using dissection.12,13 In nuce, the plastination method entails freezing the specimen at −80°C for 7 days. It is then cut into 2.5-mm-thick serial slices, with a sectioning loss of 0.9 mm of tissue. The slices are next dehydrated in 100% acetone at −30°C for 4 weeks and afterward degreased in 100% acetone at 22°C–24°C for 3 weeks. Forced impregnation of the tissue then follows and involves immersion of the slices in a vacuum chamber containing a mixture of epoxy resins (E12/E1/AE20; Biodue) at 0°C for 2 days. Finally, the plastinated slices are cured at 45°C–50°C for 5 days.14

The prepared slices were analyzed using a Leica MZ8 stereomicroscope and Leica DFC 295 digital camera (Leica Microsystems). A corollary of the plastination process is that bundles of collagen, elastin, and neurofilaments in the tissue become endogenously autofluorescent at an excitation wavelength of 488 nm, which can be detected using confocal microscopy.

3D Reconstruction

To help better understand and interpret the plastinated slices, the 3D architecture of 1 left JF was reconstructed from 32 serial ultrathin coronal sections. The skull base, first cervical vertebra, rectus capitis lateralis (RCL) muscle, and foraminal neurovascular structures were manually segmented and then reconstructed and displayed as 3D images in Amira software (version 6.9.0, Thermo Fisher Scientific).

Dural Entry Mapping

Sixty-eight jugular foramina from 34 cadaveric skull bases (24 male, 10 female; age range 57–96 years) were observed to map the dural entry points of CNs IX–XI onto a composite meatus distribution diagram.

3D Scans

Thirty dry skulls were used as a reference for the intracranial and extracranial JF bony margins. An Artec Space Spider handheld LED optical scanner (Artec 3D) was used to topographically scan the intracranial and extracranial dry skull bases. 3D skull models were generated in Artec Studio 14 Professional software.

Quantification and Statistical Analysis

Foraminal volumes of 14 jugular foramina from the 7 transverse plastinated sets were estimated by tracing the JF area on photographs of the sets using Fiji image analysis software. The JF volume was obtained by multiplying the mean traced area by the combined thickness of the slices containing the JF and dividing by 1000 to obtain volume in cubic centimeters using this equation: V = Ā × (n × 3.4)/1000, where V is the volume (cm3), Ā is the mean area, n is the slice number, and 3.4 is the total slice thickness (mm).

The total volumes of the foraminal EDNAC and internal jugular vein (IJV) subcomponents were estimated, as well as their volumes within the 3 newly described foraminal segments. A Student paired t-test was used to examine volumetric differences between the EDNAC and IJV in the total JF and within the 3 foraminal segments. The mean subtotal and total JF volumes were determined by adding the volumes of the EDNAC and IJV, and the percentage occupation of these subcomponents at each foraminal segment was calculated by dividing their respective volumes by the subtotal JF volume.

Results

Segmentation of the Jugular Foramen

Bony Landmarks

The JF was a canal-like cavity formed by the temporal and occipital bones and had an intracranial and an extracranial opening (Fig. 1). The intracranial opening was connected with the petro-occipital fissure anteromedially and the sigmoid sulcus posterolaterally and was partially divided into 2 parts by the intrajugular process of the temporal bone and the lateral ridge of the jugular tubercle of the occipital bone (Fig. 1A). CNs IX–XI entered the anterior JF after piercing the ML of the dura mater (Fig. 1B). In the majority of the specimens (91%; 62/68 foramina), CN IX was noted to enter the JF superiorly through the glossopharyngeal dural meatus and CNs X and XI to enter the JF inferiorly through a shared vagal dural meatus. The CNs were separated by an intermeatal dural septum (Fig. 1B). Two cadavers (6%; 4/68 foramina) had bilateral presentation of a common dural meatus transmitting all 3 cranial nerves (Fig. 1C), and in 1 cadaver (3%; 2/68 foramina), each nerve entered the JF via an individual dural meatus (Fig. 1D). The dural entry mapping demonstrated that the glossopharyngeal dural meatus was located anteromedially to the intrajugular process, whereas the vagal dural meatus was situated around the lateral ridge of the jugular tubercle (Fig. 1E). The extracranial opening of the JF was bordered anteriorly by the inferior margin of the jugular fossa and posteriorly by the jugular notch, which is an anterior free margin of the jugular process of the occipital bone (Fig. 1F). The intrajugular process is connected with the anterolateral edge of the jugular tubercle via fibrocartilage (Fig. 1G).

FIG. 1.
FIG. 1.

Openings of the JF. A–D: The intracranial opening without (A) and with (B–D) the dura. The blue dotted line in panels A and B outlines the JF, which is subdivided into anterior (aJF) and posterior (pJF) parts by the intrajugular process (IJP; red dot) of the temporal bone (Temp) and the lateral ridge (red dot) of the jugular tubercle (JT) of the occipital bone (Occ). E: Distribution mapping of the glossopharyngeal meatus (solid dots) and the vagal meatus (empty circles). F: The extracranial opening of the JF (blue dotted line). The red dot marks the anterolateral point of the jugular notch of the jugular process (JP). G: A transverse plastinated section at the level of the extracranial opening of the left JF, exhibiting its bipartite compartmentalization. H: A schematic diagram of the JF shown in panel G, illustrating the basic architecture of the EDNAC portion and venous portion of the JF. The crossed arrows indicate the orientation (A = anterior; M = medial). aJF = anterior part of the JF; CC = carotid canal; EL = endosteal layer of the dura; FL = foramen lacerum; FO = foramen ovale; FS = fascial sheath of the IJV; FVC = fibrovenous curtain; GF = glenoid fossa; (groove) = a groove for lower cranial nerves; HC = hypoglossal canal; IAM = internal acoustic meatus; ICA = internal carotid artery; IJP = intrajugular process; IJV = internal jugular vein; ImS = intermeatal dural septum; IPS = inferior petrosal sinus; IX = glossopharyngeal nerve; JF = jugular foramen; JP = jugular process; JT = jugular tubercle; ML = meningeal layer of the dura; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PCF = posterior condylar fossa; pJF = posterior part of the JF; POF = petro-occipital fissure; SP = styloid process; SPS = superior petrosal sulcus; SS = sigmoid sulcus; Temp = temporal bone; VII = facial nerve; VIII = vestibulocochlear nerve; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve. Bar = 3 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

Segments

The JF was subdivided into 3 segments down its length, based on 4 constant bony landmark levels (Fig. 2A–C). The first bony level was at the intracranial JF opening. The second bony level passed from the tip of the intrajugular process, parallel to the intracranial JF opening. The third bony level was drawn from the lateral lip of the extracranial JF opening to the lateral edge of the occipital condyle (Fig. 2B). The fourth line, from the mastoid process, also spanned across to the lateral edge of the occipital condyle. The areas between these levels were defined as the preforaminal, intraforaminal, and subforaminal segments of the JF (Fig. 2B).

FIG. 2.
FIG. 2.

Coronal and sagittal plastinated sections of the JF. A–C: Three adjacent coronal sections at the levels indicated by vertical dashed lines in panel E. The 4 red dashed boundary lines in B divide the JF into preforaminal (PRE), intraforaminal (INTRA), and subforaminal (SUB) segments. D–F: Three adjacent sagittal sections at the levels indicated by vertical dashed lines in panel C. The dashed circle in D outlines the ganglion of CN X. The crossed arrows indicate the orientation (S = superior; M = medial; P = posterior). ACC = anterior condylar venous confluent; ACV = anterior condylar vein; AOJ = atlanto-occipital joint; AR = arachnoid mater stained in purple color; C1 = first cervical vertebra; ICA = internal carotid artery; IJP = intrajugular process; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; IX = glossopharyngeal nerve; JB = jugular bulb; JP = jugular process; JT = jugular tubercle; ML = meningeal layer of the dura; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PCV = posterior condylar vein; RCL = rectus capitis lateralis; SP = styloid process; SS = sigmoid sinus; Temp = temporal bone; TP = transverse process; VA = vertebral artery; VV = vertebral vein; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve. Bars = 3 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

Main Contents

The anteromedial part of the JF (Fig. 2A and D) contained CNs IX–XI and the IPS, and the inferior petro-occipital vein (IPV) and anterior condylar vein (ACV) and their confluence, which drained into the jugular bulb (JB; Fig. 2B and E). CNs X and XI were located between the IPS and ACV, whereas CN IX was anterolateral to the IPS (Fig. 2B, D, and E). The posterolateral part of the JF was predominantly occupied by the JB, with some contribution from the distal SS (Fig. 2C and F).

The EDNAC Does Not Enclose the IJV

The JB of the IJV was the continuation of the distal SS (Fig. 3A and B). Its roof and floor were morphologically akin to a dural sinus, and the EL and ML of the dura were indistinguishable. Below the extracranial opening of the JF, the ML detached from the EL and contributed to the vascular fascial sheath of the IJV (Fig. 3A, C, and D). Within the JF, the ML contributed to the vascular fascial sheath on the anteromedial wall of the IJV (Figs. 3B, E, and F, and 4B and D inset) and also fanned out and continued with a dural fibrous network in the EDNAC, where an adipose matrix coexisted (Fig. 4D inset). Thus, the ML-derived dural fibrous sheath on the anteromedial wall of the IJV demarcated the JF into a large posterolateral venous portion, which contained the IJV and dura only, and a smaller anteromedial EDNAC portion, which had neurovascular structures embedded in the adipose matrix and an ML-derived dural fibrous network (Fig. 1H).

FIG. 3.
FIG. 3.

A and B: Two adjacent sagittal plastinated sections of the JF, showing the architecture of the fascial sheath of the IJV at the extracranial opening. A is lateral to B. C and D: Mirror confocal images of the box and dotted box, respectively, in panel A, showing that the meningeal dura (single arrowheads) is detached from the endosteal dura (double arrowheads). E and F: Mirror confocal images of the box and dotted box, respectively, in panel B, showing that neurovascular structures traverse the meningeal dural fibrous network (single arrowheads) and adipose matrix (asterisks) in the anterior column (yellow dotted line) and posterior column (red dotted line) of the EDNAC. The crossed arrows indicate the orientation (S = superior; P = posterior). ICA = internal carotid artery; IJV = internal jugular vein; IX = glossopharyngeal nerve; JB = jugular bulb; JP = jugular process; ML = meningeal layer of the dura; Occ = occipital bone; RCL = rectus capitis lateralis; SS = sigmoid sinus; Temp = temporal bone; v = vein; X = vagus nerve; XI = accessory nerve. Bar = 1 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

FIG. 4.
FIG. 4.

Three transverse plastinated sections at the preforaminal (A), intraforaminal (C), and subforaminal (E) levels of the JF. B, D, and F are the mirror confocal images of A, C, and E, respectively. The inset in panel D is the area of the adjacent section inferior to the box in panel D. Outlined by the yellow and red dotted lines are the anterior and posterior columns of the EDNAC, respectively. Single arrowheads indicate the meningeal dural fibrous network. Double arrowheads point to the endosteal dura. Asterisks mark the adipose tissue. The crossed arrows indicate the orientation (A = anterior; M = medial). ACC = anterior condylar confluent; ACV = anterior condylar vein; AOJ = atlanto-occipital joint; C1 = first cervical vertebra; ICA = internal carotid artery; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; IX = glossopharyngeal nerve; JB = jugular bulb; ML = meningeal layer of the dura; n = visceral nerve plexus; Occ = occipital bone; RCA = rectus capitis anterior; RCL = rectus capitis lateralis; SAS = subarachnoid space; SH = stylohyoid muscle; SP = styloid process; Temp = temporal bone; v = vein; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve; Bar = 1 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

Neurovascular and EDNAC Arrangement in the JF

In the preforaminal segment (Fig. 4A and B), the area was mainly occupied by the EDNAC, in addition to the subarachnoid space, into which CN IX and its accompanied emissary veins entered. The intermeatal dural septum (Fig. 1B) bordered CN IX posteroinferiorly, and the ML fibers detached from the EL and contributed to the neural and vascular dural sheaths (Fig. 4B).

In the intraforaminal segment (Fig. 4C and D), the IJV was positioned posterolaterally and occupied a slightly larger space in the foramen (57%; p < 0.01; Table 1) than the anteromedially positioned EDNAC, which occupied 43% of the segment (Table 1) and appeared as a quadrangular space containing the IPS, CNs IX–XI, and an adipose matrix. The IPS coursed through the space and separated CN IX anterolaterally from CNs X and XI posteromedially. The ML fibers from the intrajugular process intermingled with the fascial sheath of the IPS and extended to the occipital tubercle (Fig. 4D inset). These ML-derived fibers and the IPS formed a fibrovenous curtain that further divided the quadrangular-shaped EDNAC into a small anterior triangular column and a large posterior triangular column (Figs. 1H and 4D).

TABLE 1.

Volumetric analysis of the subcomponents of the JF

Segment SubcomponentsMean Vol in cm3 (no. of JF)JF Occupation (%)p Value
Preforaminal0.039
 EDNAC0.05 ± 0.03 (14)71%
 IJV0.02 ± 0.04 (14)29%
  Subtotal0.07 ± 0.04 (14)
Intraforaminal0.0091
 EDNAC0.49 ± 0.17 (14)43%
 IJV0.64 ± 0.22 (14)57%
  Subtotal1.13 ± 0.35 (14)
Subforaminal0.434
 EDNAC0.12 ± 0.05 (14)46%
 IJV0.14 ± 0.09 (14)54%
  Subtotal0.26 ± 0.11 (14)
Total JF0.055
 EDNAC0.66 ± 0.18 (14)45%
 IJV0.80 ± 0.28 (14)55%
  Total1.46 ± 0.39 (14)

Mean values are presented ± SD; p values are for comparison between the mean EDNAC and IJV subcomponent volumes of the JF.

In the subforaminal segment (Fig. 4E and F), the EDNAC occupied a space of similar size to that of the IJV (p > 0.05; Table 1). Compared with the intraforaminal segment, there were 2 main changes in the EDNAC anatomy. First, CN XII entered the EDNAC, and second, the fibrovenous curtain and the 2 EDNAC triangular columns extended inferiorly. The anterior EDNAC column was bordered anterolaterally by a visceral nerve plexus, which passed over the internal carotid artery and IJV and contained CN IX. The large posterior column was bordered posteromedially by the atlanto-occipital joint and the RCL and contained CNs X–XII (Figs. 1A, 3A and B, and 4E and F).

Discussion

With the use of novel epoxy sheet plastination technology in combination with confocal microscopy, this study precisely revealed the fine configuration of the dural fibrous network and its relationship with intraforaminal neurovascular and adipose structures. The main findings were the following: 1) the ML-derived vascular sheath along the anteromedial wall of the IJV demarcates the venous portion and the EDNAC portion of the bipartite JF (Fig. 1H), 2) the fibrovenous curtain formed by the ML-derived fibrous sheath and the IPS subdivides the intraforaminal EDNAC into a small anterior and a large posterior adipose column that separates CN IX from CNs X and XI, and 3) the boundaries and subdivisions of the JF can be defined by constant bony landmarks. Figure 5 is a 3D reconstruction of the JF architecture, which may serve to illustrate and aid in conceptualization of the spatial arrangement of the EDNAC and the traversing neurovascular structures in the JF and their relationships with the bony landmarks (Fig. 5A–F).

FIG. 5.
FIG. 5.

3D images of the interior and exterior of the JF. The opacity of bony structures is not presented as 100%. A: An inferolateral 3D scan of the skull base and the first cervical vertebra, C1. The rectus capitis lateralis (RCL) origin and insertion are highlighted in pink. B: A postero-infero-lateral view of a 3D image that was reconstructed from a series of the plastinated coronal sections and may mimic a posterolateral surgical approach to the JF, centered at the RCL. The asterisks mark the anterior (*) and posterior (**) parts of the EDNAC in the JF. C and D: The 3D image from the dashed box of panel B rotated 90° medially with (C) and without (D) the internal jugular vein (IJV), RCL, and anterior part of the EDNAC (*). In panel D, (JB) indicates that the jugular bulb is inside the JF and cannot be directly visualized from the interior. E and F: An interior view of the 3D JF image with (E) and without (F) the sigmoid sinus (SS), jugular bulb (JB), hypoglossal nerve (XII), anterior condylar vein (ACV), and posterior part of the EDNAC (**). The crossed arrows indicate the orientation (A = anterior; L = lateral; S = superior). C1 and C2 = first and second cervical vertebrae; CC = carotid canal; FM = foramen magnum; HC = hypoglossal canal; ICA = internal carotid artery; IJP = intrajugular process; IJV = internal jugular vein; IPS = inferior petrosal sinus; IX = glossopharyngeal nerve; JB = jugular bulb; JF = jugular foramen; JP = jugular process; JT = jugular tubercle; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PG = parotid gland; POF = petro-occipital fissure; RCL = rectus capitis lateralis; SP = styloid process; SS = sigmoid sinus; Temp = temporal bone; TF = transverse foramen; TP = transverse process; VA = vertebral artery; VII = facial nerve; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

Using Bony Landmarks to Define the Boundaries and Subdivisions of the JF

Stepwise extracranial surgical approaches to the JF have been outlined previously by Katsuta et al. (1997),15 Wen et al. (1997),16 Rhoton (2000),17 Matsushima (2015),18 and Griessenauer et al. (2016),19 among others, but these reports primarily describe procedures to access the JF and stop short at the RCL. The RCL arises from the transverse process of C1, inserts onto the jugular process, and is within the subforaminal segment of the JF (Fig. 5A and B). The subdivisions presented in this study complement previous research by detailing the anatomy within 3 newly described JF segments: preforaminal, intraforaminal, and subforaminal. All 3 segments are demarcated by bony landmarks, which are visible on medical imaging. The subdivisions proposed in this study may have a number of clinical applications. For instance, paragangliomas and meningiomas of the JF often grow in an irregular manner, and currently there is a lack of consensus on classification (in contradistinction to schwannomas).20–23 By applying the zoning presented herein, tumor classification could be based on the segment(s) occupied by the lesions within the JF, particularly when this information is combined with the distribution pattern of the venous and EDNAC portions in the individual segments. These 3 segments may also be used as operative references when accessing the JF intracranially or extracranially (Fig. 5C and D).

The EDNAC as a Feature for JF Compartmentation

The presence of the EDNAC within the JF has been designated as a foraminal compartment by Bernard et al., who demonstrated that CNs IX–XI and the IPS, distal SS, and IJV and their dural sheaths course within the EDNAC of the JF.6 Bernard et al. group the IPS and IJV within the same “interperiosteodural compartment” and separate CN IX from CNs X and XI by an “intrajugular ligament,” resulting in the proposal of a 3-part compartmentation of the JF.6,11 The findings of our study indicate that the IJV is actually not part of the EDNAC, as there is no adipose space between the wall of the IJV and the periosteum intraforaminally. Accordingly, this observation contradicts the inclusion of the IJV with the EDNAC in the Bernard et al. model.6 The ML of the dura that passes over the anteromedial wall of the IJV bridges between the intrajugular process of the temporal bone and the jugular tubercle of the occipital bone, and thus effectively forms a bipartite foramen containing a venous and an EDNAC portion (Fig. 1H). Except for the preforaminal segment, these 2 portions occupy a space of a more or less similar size, although in the intraforaminal segment, the venous portion is slightly larger than the EDNAC portion (57% vs 43%).

The bipartite compartmentation proposed in this study is virtually identical to the model proposed by Shapiro (1972).11,24 The main difference between the 2 proposed models is that the compartmentation proposed by Shapiro was based on the EDNAC and IJV contents rather than the central bony JF constriction visible on radiographs. An influential early proposal of JF compartmentation by Hovelacque (1934) placed the IPS and CN IX into the anterior half, and CNs X and XI and the IJV in the posterior half.11,25 Yet another JF model, by Katsuta et al., assigned an anterior part to the IPS, a middle part to all 3 cranial nerves, and a posterior compartment for the IJV.11,15 Both Hovelacque and Katsuta et al. designated a separate compartment for the IPS. However, the IPS constitutes a venous element that is prevalent throughout the EDNAC; therefore, as depicted in our model, the IPS should be classed along with the cranial nerves in the EDNAC and not separated from them.

Structural Septa Within the EDNAC of the Jugular Foramen

Within the JF, Bernard et al. defined the dural fibrous thickenings anterior and posterior to CN IX as an intrajugular ligament and believed it may serve as a surgical barrier to protect the lower cranial nerves, but the authors noted that it was impossible to ascertain macroscopically the configuration and origin of the intrajugular ligament.6 It has been reported that in the cavernous sinus, the traversing neurovascular structures are supported by an adipose matrix and a dural fibrous network that originates from the ML of the dura, continues with neurovascular sheaths, and terminates in the adipose matrix, forming a “skeleton frame” within the EDNAC.12 As shown in the present study, the EDNAC in the JF is dominated by the ML-derived fibrous network. The ML fibers in the EDNAC are orientated in 2 general directions, either longitudinally along the neurovascular structures as the dural sheath of a vessel or nerve, or transversely between the temporal and occipital bones. These 2 types of ML fibers intermingle around the IPS, superiorly connecting with the intermeatal septum and inferiorly extending to the fascial sheath of the ACV and confluence and the IJV. Therefore, together with the IPS, they are termed a fibrovenous curtain in the present study.

The fibrovenous curtain of the JF divides the EDNAC into a small anterior and a large posterior column (Fig. 1H). The anterior EDNAC column contains CN IX and the anterior condylar venous complex, while the posterior EDNAC column transmits CNs X–XII. Figure 5C and D highlights the RCL as a crucial landmark to access these 2 EDNAC columns extracranially. Intracranial dural mapping of the nerve entry points reported in this study may be used as the “intracranial gates of access” to these 2 columns in the JF (Fig. 5E and F). Care should be taken with structural generalization, and individual anatomical variation should be considered. Variations from the “normal” 2-meatus dural septation (91%) to single (6%) or triple (3%) dural septation patterns observed in the present study correspond to observations and classifications made by Tubbs et al. (2015).26

Clinical Considerations of the EDNAC Configuration in the JF

JF tumors are rare27 and are divided into 2 categories, intrinsic (primary) tumors originating within the JF itself and extrinsic (secondary) tumors that penetrate the JF from neighboring areas.21,28 In order of frequency, the main intrinsic JF tumors are glomus jugulare tumors, schwannomas, and meningiomas, and these can arise near the IPS, within the lower cranial nerves, or from the JB.27,29 Metastatic tumors, chordomas, and chondrosarcomas are examples of extrinsic tumors that very infrequently invade the JF from the clivus, the cerebellopontine angle, or the foramen magnum.21,28,29 Based on the JF compartmentation presented herein, schwannomas and meningiomas would most likely be located in the EDNAC portion, while the glomus jugular would originate within the vascular portion of the JF.29 Song et al. (2008) postulated that the intraforaminal IPS may act as a barrier for tumor expansion, impeding either upward encroachment of extracranial tumors or downward growth of intracranial lesions.30 The intraforaminal fibrovenous curtain defined in this study, in addition to limiting tumor expansion superiorly and inferiorly, may also restrict tumor growth to be contained within its anterolateral or posteromedial EDNAC column, depending on the tumor origin site. For example, a schwannoma of CN IX would be contained within the anteromedial column, and conversely, a schwannoma of CN X or XI would be confined to the posterolateral column. These suggested mechanical barriers may be particularly relevant to the tumor morphology observed in JF schwannomas. Samii et al. (1995) classified JF schwannomas into type A (with minimal JF encroachment), type B (within the JF with an intracranial extension), type C (mainly extracranial with a JF extension), and type D (dumbbell shaped with both intra- and extracranial segments).20 It is conceivable that type A and B tumors are contained by the IPS inferiorly and type C tumors by the IPS superiorly. The integrity of the limiting fibrovenous curtain may be compromised in the case of type D (dumbbell) schwannomas, allowing unencumbered tumor growth and burgeoning at both ends of the JF. Cases such as this demonstrate that understanding of this vascular and dural relationship within the JF may provide a means to predict the growth pattern of tumors in this area and thus inform operative approaches.

The EDNAC may communicate with the perineural tumor spread (PNS) pathway. The PNS is a recognized pattern of tumor dissemination occurring along the potential space between the nerve and its coverings, e.g., the perineurium and epineurium, and is associated with risk of tumor recurrence and higher morbidity and mortality.31 The epineurium is a continuation of the ML and lies between the internal epineurium and around the external epineurium nerve fascicles (or trunks). In the cavernous sinus, the ML-derived epineurium of the traversing cranial nerves gradually fans out and continues with the adipose network.12 Figures 3F and 4E of this study and Fig. 3E of the Liang et al. report10 show that the adipose tissue within the epineurium of CNs X and XI communicates freely with the EDNAC in the JF.

Study Limitations

Two limitations were identified in this study: 1) only cadavers of older adults (age range 57–96 years) were used, and 2) observational and quantitative measurements were conducted only on a small sample. The EDNAC contains abundant fat; therefore, fatty atrophy in specimens from older adults may reduce EDNAC dimensions, resulting in an evaluation of EDNAC size and volume that is not reflective of younger individuals. In addition to individual variation of the intracranial dural meatuses, the components and patterns of the anterior condylar venous complex vary considerably, which may alter the configuration of the dural fibrous network in the JF.32,33

Conclusions

This study is a systematic exploration of the EDNAC within the JF and has confirmed that the EDNAC does not surround the IJV. Instead, have we presented a novel bipartite compartmentation of the JF and revealed that a fibrovenous curtain in the JF further subdivides the foraminal EDNAC into a small anterior and a large posterior column. Investigating the EDNAC within the JF is important, as it will contribute to our knowledge of this obscure yet crucially important anatomical region. Additionally, such research will improve our understanding of foraminal tumor growth and spread patterns and planning and execution of surgical interventions in this region.20,22

Acknowledgments

We would like to thank Robbie McPhee, Medical Illustrator and Graphic Artist (University of Otago, Department of Anatomy), for his artwork contributions. We are also grateful to Paddy Cheah for scanning the skull bases and generating the 3D skull models.

This project was funded by a University of Otago Research Grant (reference no. 2018-2020) and the National Natural Science Foundation of China (reference no. 81671368).

Disclosures

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

Author Contributions

Conception and design: Zhang, Bond. Acquisition of data: all authors. Analysis and interpretation of data: Zhang, Bond. Drafting the article: Bond. Critically revising the article: Zhang, Bond. Reviewed submitted version of manuscript: Zhang, Bond. Approved the final version of the manuscript on behalf of all authors: Zhang. Statistical analysis: Bond. Study supervision: Zhang.

References

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  • 2

    François P , Zemmoura I , Fouquet AMB , et al. . Lateral sellar angiolipoma: a tumor illustrative of the extradural compartment of the neural axis . J Neurosurg . 2010 ;113 (5 ):1053 1058 .

    • Search Google Scholar
    • Export Citation
  • 3

    Parkinson D . History of the extradural neural axis compartment . Surg Neurol . 2000 ;54 (6 ):422 431 .

  • 4

    Zamboni P , Consorti G , Galeotti R , et al. . Venous collateral circulation of the extracranial cerebrospinal outflow routes . Curr Neurovasc Res . 2009 ;6 (3 ):204 212 .

    • Search Google Scholar
    • Export Citation
  • 5

    Sakka L , Gabrillargues J , Coll G . Anatomy of the spinal meninges . Oper Neurosurg (Hagerstown). 2016 ;12 (2 ):168 188 .

  • 6

    Bernard F , Zemmoura I , Cottier JP , et al. . The interperiosteodural concept applied to the jugular foramen and its compartmentalization . J Neurosurg . 2018 ;129 (3 ):770 778 .

    • Search Google Scholar
    • Export Citation
  • 7

    François P , Travers N , Lescanne E , et al. . The interperiosteodural concept applied to the perisellar compartment: a microanatomical and electron microscopic study . J Neurosurg . 2010 ;113 (5 ):1045 1052 .

    • Search Google Scholar
    • Export Citation
  • 8

    François P , Lescanne E , Velut S . The dural sheath of the optic nerve: descriptive anatomy and surgical applications . Adv Tech Stand Neurosurg . 2011 ;36 :187 198 .

    • Search Google Scholar
    • Export Citation
  • 9

    Xu Z , Lin G , Zhang H , et al. . Three-dimensional architecture of the neurovascular and adipose zones of the upper and lower lumbar intervertebral foramina: an epoxy sheet plastination study . J Neurosurg Spine . 2020 ;32 (5 ):722 732 .

    • Search Google Scholar
    • Export Citation
  • 10

    Liang L , Qu L , Chu X , et al. . Meningeal architecture of the jugular foramen: an anatomic study using plastinated histologic sections . World Neurosurg . 2019 ;127 :e809 e817 .

    • Search Google Scholar
    • Export Citation
  • 11

    Bond JD , Zhang M . Compartmental subdivisions of the jugular foramen: a review of the current models . World Neurosurg . 2020 ;136 :49 57 .

    • Search Google Scholar
    • Export Citation
  • 12

    Liang L , Gao F , Xu Q , Zhang M . Configuration of fibrous and adipose tissues in the cavernous sinus . PLoS One . 2014 ;9 (2 ):e89182 .

    • Search Google Scholar
    • Export Citation
  • 13

    Liugan M , Xu Z , Zhang M . Reduced free communication of the subarachnoid space within the optic canal in the human . Am J Ophthalmol . 2017 ;179 :25 31 .

    • Search Google Scholar
    • Export Citation
  • 14

    von Hagens G , Tiedemann K , Kriz W . The current potential of plastination . Anat Embryol (Berl) . 1987 ;175 (4 ):411 421 .

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    Katsuta T , Rhoton AL Jr , Matsushima T . The jugular foramen: microsurgical anatomy and operative approaches . Neurosurgery . 1997 ;41 (1 ):149 202 .

    • Search Google Scholar
    • Export Citation
  • 16

    Wen HT , Rhoton AL Jr , Katsuta T , de Oliveira E . Microsurgical anatomy of the transcondylar, supracondylar, and paracondylar extensions of the far-lateral approach . J Neurosurg . 1997 ;87 (4 ):555 585 .

    • Search Google Scholar
    • Export Citation
  • 17

    Rhoton AL Jr. Jugular foramen. Neurosurgery. 2000 ;47(3) (suppl):S267 S285 .

  • 18

    Matsushima T. Microsurgical anatomy of and surgical approaches to the jugular foramen . In: Microsurgical Anatomy and Surgery of the Posterior Cranial Fossa . Springer ; 2015 :277 297 .

    • Search Google Scholar
    • Export Citation
  • 19

    Griessenauer CJ , McGrew B , Matusz P , et al. . Surgical approaches to the jugular foramen: a comprehensive review . J Neurol Surg B Skull Base . 2016 ;77 (3 ):260 264 .

    • Search Google Scholar
    • Export Citation
  • 20

    Samii M , Babu RP , Tatagiba M , Sepehrnia A . Surgical treatment of jugular foramen schwannomas . J Neurosurg . 1995 ;82 (6 ):924 932 .

    • Search Google Scholar
    • Export Citation
  • 21

    Vogl TJ , Bisdas S . Differential diagnosis of jugular foramen lesions . Skull Base . 2009 ;19 (1 ):3 16 .

  • 22

    Sutiono AB , Kawase T , Tabuse M , et al. . Importance of preserved periosteum around jugular foramen neurinomas for functional outcome of lower cranial nerves: anatomic and clinical studies . Oper Neurosurg (Hagerstown) . 2011 ;69 :ons230 ons240 .

    • Search Google Scholar
    • Export Citation
  • 23

    Bakar B. The jugular foramen schwannomas: review of the large surgical series . J Korean Neurosurg Soc . 2008 ;44 (5 ):285 294 .

    • Search Google Scholar
    • Export Citation
  • 24

    Shapiro R . Compartmentation of the jugular foramen . J Neurosurg . 1972 ;36 (3 ):340 343 .

  • 25

    Hovelacque A . Le crâne dans son ensemble . In: Ostéologie . Vol. 2. Doin and Cie ; 1934 :155 156 .

  • 26

    Tubbs RS , Griessenauer CJ , Bilal M , et al. . Dural septation on the inner surface of the jugular foramen: an anatomical study . J Neurol Surg B Skull Base . 2015 ;76 (3 ):214 217 .

    • Search Google Scholar
    • Export Citation
  • 27

    Ramina R , Maniglia JJ , Fernandes YB , et al. . Jugular foramen tumors: diagnosis and treatment . Neurosurg Focus . 2004 ;17 (2 ):E5 .

  • 28

    Guinto G , Kageyama M , Trujillo-Luarca VH , et al. . Nonglomic tumors of the jugular foramen: differential diagnosis and prognostic implications . World Neurosurg . 2014 ;82 (6 ):1283 1290 .

    • Search Google Scholar
    • Export Citation
  • 29

    Lustig LR , Jackler RK . The variable relationship between the lower cranial nerves and jugular foramen tumors: implications for neural preservation . Am J Otol . 1996 ;17 (4 ):658 668 .

    • Search Google Scholar
    • Export Citation
  • 30

    Song MH , Lee HY , Jeon JS , et al. . Jugular foramen schwannoma: analysis on its origin and location . Otol Neurotol . 2008 ;29 (3 ):387 391 .

    • Search Google Scholar
    • Export Citation
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    Badger D , Aygun N . Imaging of perineural spread in head and neck cancer . Radiol Clin North Am . 2017 ;55 (1 ):139 149 .

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    Tubbs RS , Watanabe K , Loukas M , Cohen-Gadol AA . Anatomy of the inferior petro-occipital vein and its relation to the base of the skull: application to surgical and endovascular procedures of the skull base . Clin Anat . 2014 ;27 (5 ):698 701 .

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Illustrations from Marx and Schroeder (pp 318–326). Copyright Henry W. S. Schroeder. Published with permission.
  • View in gallery

    Openings of the JF. A–D: The intracranial opening without (A) and with (B–D) the dura. The blue dotted line in panels A and B outlines the JF, which is subdivided into anterior (aJF) and posterior (pJF) parts by the intrajugular process (IJP; red dot) of the temporal bone (Temp) and the lateral ridge (red dot) of the jugular tubercle (JT) of the occipital bone (Occ). E: Distribution mapping of the glossopharyngeal meatus (solid dots) and the vagal meatus (empty circles). F: The extracranial opening of the JF (blue dotted line). The red dot marks the anterolateral point of the jugular notch of the jugular process (JP). G: A transverse plastinated section at the level of the extracranial opening of the left JF, exhibiting its bipartite compartmentalization. H: A schematic diagram of the JF shown in panel G, illustrating the basic architecture of the EDNAC portion and venous portion of the JF. The crossed arrows indicate the orientation (A = anterior; M = medial). aJF = anterior part of the JF; CC = carotid canal; EL = endosteal layer of the dura; FL = foramen lacerum; FO = foramen ovale; FS = fascial sheath of the IJV; FVC = fibrovenous curtain; GF = glenoid fossa; (groove) = a groove for lower cranial nerves; HC = hypoglossal canal; IAM = internal acoustic meatus; ICA = internal carotid artery; IJP = intrajugular process; IJV = internal jugular vein; ImS = intermeatal dural septum; IPS = inferior petrosal sinus; IX = glossopharyngeal nerve; JF = jugular foramen; JP = jugular process; JT = jugular tubercle; ML = meningeal layer of the dura; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PCF = posterior condylar fossa; pJF = posterior part of the JF; POF = petro-occipital fissure; SP = styloid process; SPS = superior petrosal sulcus; SS = sigmoid sulcus; Temp = temporal bone; VII = facial nerve; VIII = vestibulocochlear nerve; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve. Bar = 3 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

  • View in gallery

    Coronal and sagittal plastinated sections of the JF. A–C: Three adjacent coronal sections at the levels indicated by vertical dashed lines in panel E. The 4 red dashed boundary lines in B divide the JF into preforaminal (PRE), intraforaminal (INTRA), and subforaminal (SUB) segments. D–F: Three adjacent sagittal sections at the levels indicated by vertical dashed lines in panel C. The dashed circle in D outlines the ganglion of CN X. The crossed arrows indicate the orientation (S = superior; M = medial; P = posterior). ACC = anterior condylar venous confluent; ACV = anterior condylar vein; AOJ = atlanto-occipital joint; AR = arachnoid mater stained in purple color; C1 = first cervical vertebra; ICA = internal carotid artery; IJP = intrajugular process; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; IX = glossopharyngeal nerve; JB = jugular bulb; JP = jugular process; JT = jugular tubercle; ML = meningeal layer of the dura; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PCV = posterior condylar vein; RCL = rectus capitis lateralis; SP = styloid process; SS = sigmoid sinus; Temp = temporal bone; TP = transverse process; VA = vertebral artery; VV = vertebral vein; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve. Bars = 3 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

  • View in gallery

    A and B: Two adjacent sagittal plastinated sections of the JF, showing the architecture of the fascial sheath of the IJV at the extracranial opening. A is lateral to B. C and D: Mirror confocal images of the box and dotted box, respectively, in panel A, showing that the meningeal dura (single arrowheads) is detached from the endosteal dura (double arrowheads). E and F: Mirror confocal images of the box and dotted box, respectively, in panel B, showing that neurovascular structures traverse the meningeal dural fibrous network (single arrowheads) and adipose matrix (asterisks) in the anterior column (yellow dotted line) and posterior column (red dotted line) of the EDNAC. The crossed arrows indicate the orientation (S = superior; P = posterior). ICA = internal carotid artery; IJV = internal jugular vein; IX = glossopharyngeal nerve; JB = jugular bulb; JP = jugular process; ML = meningeal layer of the dura; Occ = occipital bone; RCL = rectus capitis lateralis; SS = sigmoid sinus; Temp = temporal bone; v = vein; X = vagus nerve; XI = accessory nerve. Bar = 1 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

  • View in gallery

    Three transverse plastinated sections at the preforaminal (A), intraforaminal (C), and subforaminal (E) levels of the JF. B, D, and F are the mirror confocal images of A, C, and E, respectively. The inset in panel D is the area of the adjacent section inferior to the box in panel D. Outlined by the yellow and red dotted lines are the anterior and posterior columns of the EDNAC, respectively. Single arrowheads indicate the meningeal dural fibrous network. Double arrowheads point to the endosteal dura. Asterisks mark the adipose tissue. The crossed arrows indicate the orientation (A = anterior; M = medial). ACC = anterior condylar confluent; ACV = anterior condylar vein; AOJ = atlanto-occipital joint; C1 = first cervical vertebra; ICA = internal carotid artery; IJV = internal jugular vein; IPS = inferior petrosal sinus; IPV = inferior petro-occipital vein; IX = glossopharyngeal nerve; JB = jugular bulb; ML = meningeal layer of the dura; n = visceral nerve plexus; Occ = occipital bone; RCA = rectus capitis anterior; RCL = rectus capitis lateralis; SAS = subarachnoid space; SH = stylohyoid muscle; SP = styloid process; Temp = temporal bone; v = vein; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve; Bar = 1 mm. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

  • View in gallery

    3D images of the interior and exterior of the JF. The opacity of bony structures is not presented as 100%. A: An inferolateral 3D scan of the skull base and the first cervical vertebra, C1. The rectus capitis lateralis (RCL) origin and insertion are highlighted in pink. B: A postero-infero-lateral view of a 3D image that was reconstructed from a series of the plastinated coronal sections and may mimic a posterolateral surgical approach to the JF, centered at the RCL. The asterisks mark the anterior (*) and posterior (**) parts of the EDNAC in the JF. C and D: The 3D image from the dashed box of panel B rotated 90° medially with (C) and without (D) the internal jugular vein (IJV), RCL, and anterior part of the EDNAC (*). In panel D, (JB) indicates that the jugular bulb is inside the JF and cannot be directly visualized from the interior. E and F: An interior view of the 3D JF image with (E) and without (F) the sigmoid sinus (SS), jugular bulb (JB), hypoglossal nerve (XII), anterior condylar vein (ACV), and posterior part of the EDNAC (**). The crossed arrows indicate the orientation (A = anterior; L = lateral; S = superior). C1 and C2 = first and second cervical vertebrae; CC = carotid canal; FM = foramen magnum; HC = hypoglossal canal; ICA = internal carotid artery; IJP = intrajugular process; IJV = internal jugular vein; IPS = inferior petrosal sinus; IX = glossopharyngeal nerve; JB = jugular bulb; JF = jugular foramen; JP = jugular process; JT = jugular tubercle; MP = mastoid process; OC = occipital condyle; Occ = occipital bone; PG = parotid gland; POF = petro-occipital fissure; RCL = rectus capitis lateralis; SP = styloid process; SS = sigmoid sinus; Temp = temporal bone; TF = transverse foramen; TP = transverse process; VA = vertebral artery; VII = facial nerve; X = vagus nerve; XI = accessory nerve; XII = hypoglossal nerve. Copyright Ming Zhang. Published with permission. Figure is available in color online only.

  • 1

    Parkinson D . Extradural neural axis compartment . J Neurosurg . 2000 ;92 (4 ):585 588 .

  • 2

    François P , Zemmoura I , Fouquet AMB , et al. . Lateral sellar angiolipoma: a tumor illustrative of the extradural compartment of the neural axis . J Neurosurg . 2010 ;113 (5 ):1053 1058 .

    • Search Google Scholar
    • Export Citation
  • 3

    Parkinson D . History of the extradural neural axis compartment . Surg Neurol . 2000 ;54 (6 ):422 431 .

  • 4

    Zamboni P , Consorti G , Galeotti R , et al. . Venous collateral circulation of the extracranial cerebrospinal outflow routes . Curr Neurovasc Res . 2009 ;6 (3 ):204 212 .

    • Search Google Scholar
    • Export Citation
  • 5

    Sakka L , Gabrillargues J , Coll G . Anatomy of the spinal meninges . Oper Neurosurg (Hagerstown). 2016 ;12 (2 ):168 188 .

  • 6

    Bernard F , Zemmoura I , Cottier JP , et al. . The interperiosteodural concept applied to the jugular foramen and its compartmentalization . J Neurosurg . 2018 ;129 (3 ):770 778 .

    • Search Google Scholar
    • Export Citation
  • 7

    François P , Travers N , Lescanne E , et al. . The interperiosteodural concept applied to the perisellar compartment: a microanatomical and electron microscopic study . J Neurosurg . 2010 ;113 (5 ):1045 1052 .

    • Search Google Scholar
    • Export Citation
  • 8

    François P , Lescanne E , Velut S . The dural sheath of the optic nerve: descriptive anatomy and surgical applications . Adv Tech Stand Neurosurg . 2011 ;36 :187 198 .

    • Search Google Scholar
    • Export Citation
  • 9

    Xu Z , Lin G , Zhang H , et al. . Three-dimensional architecture of the neurovascular and adipose zones of the upper and lower lumbar intervertebral foramina: an epoxy sheet plastination study . J Neurosurg Spine . 2020 ;32 (5 ):722 732 .

    • Search Google Scholar
    • Export Citation
  • 10

    Liang L , Qu L , Chu X , et al. . Meningeal architecture of the jugular foramen: an anatomic study using plastinated histologic sections . World Neurosurg . 2019 ;127 :e809 e817 .

    • Search Google Scholar
    • Export Citation
  • 11

    Bond JD , Zhang M . Compartmental subdivisions of the jugular foramen: a review of the current models . World Neurosurg . 2020 ;136 :49 57 .

    • Search Google Scholar
    • Export Citation
  • 12

    Liang L , Gao F , Xu Q , Zhang M . Configuration of fibrous and adipose tissues in the cavernous sinus . PLoS One . 2014 ;9 (2 ):e89182 .

    • Search Google Scholar
    • Export Citation
  • 13

    Liugan M , Xu Z , Zhang M . Reduced free communication of the subarachnoid space within the optic canal in the human . Am J Ophthalmol . 2017 ;179 :25 31 .

    • Search Google Scholar
    • Export Citation
  • 14

    von Hagens G , Tiedemann K , Kriz W . The current potential of plastination . Anat Embryol (Berl) . 1987 ;175 (4 ):411 421 .

  • 15

    Katsuta T , Rhoton AL Jr , Matsushima T . The jugular foramen: microsurgical anatomy and operative approaches . Neurosurgery . 1997 ;41 (1 ):149 202 .

    • Search Google Scholar
    • Export Citation
  • 16

    Wen HT , Rhoton AL Jr , Katsuta T , de Oliveira E . Microsurgical anatomy of the transcondylar, supracondylar, and paracondylar extensions of the far-lateral approach . J Neurosurg . 1997 ;87 (4 ):555 585 .

    • Search Google Scholar
    • Export Citation
  • 17

    Rhoton AL Jr. Jugular foramen. Neurosurgery. 2000 ;47(3) (suppl):S267 S285 .

  • 18

    Matsushima T. Microsurgical anatomy of and surgical approaches to the jugular foramen . In: Microsurgical Anatomy and Surgery of the Posterior Cranial Fossa . Springer ; 2015 :277 297 .

    • Search Google Scholar
    • Export Citation
  • 19

    Griessenauer CJ , McGrew B , Matusz P , et al. . Surgical approaches to the jugular foramen: a comprehensive review . J Neurol Surg B Skull Base . 2016 ;77 (3 ):260 264 .

    • Search Google Scholar
    • Export Citation
  • 20

    Samii M , Babu RP , Tatagiba M , Sepehrnia A . Surgical treatment of jugular foramen schwannomas . J Neurosurg . 1995 ;82 (6 ):924 932 .

    • Search Google Scholar
    • Export Citation
  • 21

    Vogl TJ , Bisdas S . Differential diagnosis of jugular foramen lesions . Skull Base . 2009 ;19 (1 ):3 16 .

  • 22

    Sutiono AB , Kawase T , Tabuse M , et al. . Importance of preserved periosteum around jugular foramen neurinomas for functional outcome of lower cranial nerves: anatomic and clinical studies . Oper Neurosurg (Hagerstown) . 2011 ;69 :ons230 ons240 .

    • Search Google Scholar
    • Export Citation
  • 23

    Bakar B. The jugular foramen schwannomas: review of the large surgical series . J Korean Neurosurg Soc . 2008 ;44 (5 ):285 294 .

    • Search Google Scholar
    • Export Citation
  • 24

    Shapiro R . Compartmentation of the jugular foramen . J Neurosurg . 1972 ;36 (3 ):340 343 .

  • 25

    Hovelacque A . Le crâne dans son ensemble . In: Ostéologie . Vol. 2. Doin and Cie ; 1934 :155 156 .

  • 26

    Tubbs RS , Griessenauer CJ , Bilal M , et al. . Dural septation on the inner surface of the jugular foramen: an anatomical study . J Neurol Surg B Skull Base . 2015 ;76 (3 ):214 217 .

    • Search Google Scholar
    • Export Citation
  • 27

    Ramina R , Maniglia JJ , Fernandes YB , et al. . Jugular foramen tumors: diagnosis and treatment . Neurosurg Focus . 2004 ;17 (2 ):E5 .

  • 28

    Guinto G , Kageyama M , Trujillo-Luarca VH , et al. . Nonglomic tumors of the jugular foramen: differential diagnosis and prognostic implications . World Neurosurg . 2014 ;82 (6 ):1283 1290 .

    • Search Google Scholar
    • Export Citation
  • 29

    Lustig LR , Jackler RK . The variable relationship between the lower cranial nerves and jugular foramen tumors: implications for neural preservation . Am J Otol . 1996 ;17 (4 ):658 668 .

    • Search Google Scholar
    • Export Citation
  • 30

    Song MH , Lee HY , Jeon JS , et al. . Jugular foramen schwannoma: analysis on its origin and location . Otol Neurotol . 2008 ;29 (3 ):387 391 .

    • Search Google Scholar
    • Export Citation
  • 31

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