The Relationship Between Jugular Foramen Schwannoma and Surrounding Membrane Structures and Its Surgical Application

Abstract

Background and objectives: Surgical resection of jugular foramen (JF) schwannomas with minimal neurological complications is challenging because of their difficult-to-access location and complex relationships with surrounding neurovascular structures, even for experienced neurosurgeons. In this article, we elucidate the membranous anatomy of JF schwannomas, with the aim of reducing iatrogenic injury to the lower cranial nerves (LCNs) during surgery.

Methods: The clinical data of 31 consecutive patients with JF schwannomas were reviewed. The relationship between the tumor and the surrounding membranous structures was observed during dissection. Samples were analyzed using Masson's trichrome and immunofluorescence staining to study the membranous characteristics. Histological-radiographic correlations were also summarized.

Results: In this series, we found that all 3 type B, 2 type C, and 8 type D tumors (according to the Kaye-Pellet grading system) were entirely extradural in location, whereas the 18 type A tumors could be subdural (9 cases) or extradural (9 cases), which frequently could not be predicted preoperatively based on whether the tumor had intraforaminal extension. The dural capsule, when present, could be used as an insulating layer to protect LCNs. With this subcapsular dissection technique, postoperative LCN dysfunction occurred in 10 patients (32.3%), which was usually temporary and mild.

Conclusion: The different relationships between the tumor and membranous structures of the JF is related to the distinct point of tumor origin and the complex anatomy of the meningeal dura within the JF. Subcapsular dissection technique is recommended for better preservation of LCNs when the dural capsule is identified.

Keywords: Arachnoid; Case series; Dura mater; Jugular foramen; Schwannoma; Surgery.

FIGURE 1.

Intraoperative images showing the distribution of LCNs. A and B, A large number of LCN rootlets (white arrows) were found on the upper part of the intracranial tumor, and the CN XI was confirmed as the originating nerve. The white asterisk in B, indicates the dural capsule. C, This tumor originated from CN glossopharyngeal nerve, and most of the LCN rootlets (white arrows) gathered at the inferior pole of the tumor. Sides of lesions were labeled as L (left) and R (right). CN, cranial nerve; LCN, lower CN; XI, accessory nerve.

FIGURE 2.

Intraoperative images of subdural jugular foramen schwannomas. The intracranial tumors had no dural capsule. The spinal accessory nerve was constantly located at the inferior pole of the tumor, but other lower cranial nerves could be pushed to any direction. A, The IX nerve, X nerve, and cranial roots of XI nerve were located at different directions of the tumor. B, All the IX nerve, X nerve, and cranial roots of XI nerve were found on the posterior surface of the tumor. T, tumor; IX, glossopharyngeal nerve; X, vagus nerve; XI, accessory nerve. Sides of lesions were labeled as L (left) and R (right).

FIGURE 3.

Photomicrographs of a subdural sample. There was no sign of dura mater on the free surface of the tumor. A, Low-magnification image of MT staining. High-magnification images of B, Masson's trichrome and C and D, immunofluorescence staining of the red-framed area in image A. Tumor was positively stained by S100, whereas nerve fibers were positively stained by neurofilament and myelin basic protein. DAPI, 4',6-diamidino-2-phenylindole; MBP, myelin basic protein; NF, neurofibromatosis.

FIGURE 4.

Intraoperative images of extradural JF schwannomas. The intracranial parts of the tumors were entirely encased by the dural capsule with active angiogenesis. The dural capsule might be A, thin and translucent or B, thick and whitish. White arrowheads in A, indicate the cutting edge of the dural capsule at the intracranial orifice of the JF, whereas black arrows indicate the fold of arachnoid. C-E, Photographs showing the crater-like dural invagination (black asterisk) along the edge of JF. It most commonly appeared at the C, posteroinferior part of the dural capsule and occasionally at the D and E, posterosuperior part. The dural invagination could serve as a reliable indicator for locating the LCNs (white arrows). F, Image showing 2 dural layers (white arrowheads) on the surface of the tumor near the intracranial JF opening, with LCN rootlets (white arrow) between them. X, vagus nerve; XI, accessory nerve. Sides of lesions were labeled as L (left) and R (right). JF, jugular foramen; LCNs, lower cranial nerves.

FIGURE 5.

Photomicrographs of extradural samples. Tumors were covered by dura mater (black arrows). A and C, MT and B and D, IF staining showing a significant difference in thickness of the dural capsule between 2 extradural tumors. E, Low-magnification image of MT staining showing the dural capsule had encased the entire intracranial tumor. High-magnification images of F, MT and G and H, IF staining of the red-framed area in E. There were 2 layers of dura mater (red dotted line indicated the boundary) at the peripheral part of the dural capsule, with nerve fibers (black arrowheads) between them. Nerve fibers were positively stained by NF and MBP, and tumor was positively stained by S100, whereas dura mater was stained negative by all these markers. DAPI, 4',6-diamidino-2-phenylindole; IF, immunofluorescence; MBP, myelin basic protein; MT, Masson's trichrome; NF, neurofilament.

FIGURE 6.

Variety of membranous characteristics in Kaye-Pellet type A tumors. A, Preoperative contrast-enhanced T1-weighted MRI showed a small round lesion in cerebellopontine cistern without JF involvement, and B, it was demonstrated to be a subdural tumor intraoperatively. C-E. Preoperative thin-sliced T2-weighted MRI revealed that the tumor just filled the recess of vagus meatus (D, white arrowhead) but did not involve the glossopharyngeal meatus (C, red arrowhead). E, Intraoperatively, the tumor has a distinct dural capsule with active angiogenesis. F, Preoperative contrast-enhanced T1-weighted MRI showed that the tumor had deeply extended into the JF, yet G, the intracranial tumor had no dural capsule. JF, jugular foramen.

FIGURE 7.

Schematic drawings showing different growth patterns of JF schwannomas depending on their exact origin in relationship to the membranous structures of the JF. Tumor originating from the proximal intraforaminal segment of LCNs (origin points 1 and 2) may grow into the subdural space under the guidance of the dural sheath. On the contrary, tumor arising from the distal intraforaminal segment (origin points 3, 4, and 5) would develop into extradural tumor eventually. When the tumor originates from the distal intraforaminal segment of the IX nerve (origin point 3), the dural sheath is expanded and folds on the horizontal segment as the tumor extends intracranially. If the tumor origin locates deeply inside the JF (origin points 3 and 5), the dura at the edge of the intracranial opening of the JF may be expanded subsequently and becomes the peripheral part of the dural capsule as the tumor extends intracranially. In this scenario, the remaining rootlets of the LCN are sandwiched between the peripheral and dome parts of the dural capsule. IX, glossopharyngeal nerve; X, vagus nerve; XI, accessory nerve. The copyright of Figure 7 belongs to Xi'an Zhang. JF, jugular foramen; LCNs, lower cranial nerves.