Surgical treatment of selected tumors via the navigated minimally invasive presigmoidal suprabulbar infralabyrinthine approach without rerouting of the facial nerve

The feasibility of a novel skull base approach — the navigated minimally invasive presigmoidal suprabulbar infralabyrinthine approach (NaMIPSI-A) without rerouting of the fallopian canal for selected jugular foramen tumors (JFTs) — has been demonstrated in a neuroanatomical laboratory study. Here, we present our clinical experience with the NaMIPSI-A for selected JFTs, with a particular focus on its efficacy and safety. All patients with JFTs who were treated via the NaMIPSI-A were included in this study. The JFTs were classified according to a modified Fisch classification. The neurological and neuroradiological outcome, the extent of tumor resection, and the approach-related morbidity were examined. Five patients (two women, three men; mean age 57 years, range 48–65) were available. According to the modified Fisch classification, two JFTs were graded as C1, one as De1, and two as De2. Gross total resection (GTR) was achieved in three patients and near-total resection (NTR) in two. Postsurgically, no new neurological deficits and no approach-related morbidity and mortality occurred. One case with a postoperative cerebrospinal fluid leak was managed successfully with lumbar drainage. During the follow-up period (mean 67.6 months, range 12–119 months), tumor recurrence was noted in the NTR group but not in the GTR group. The NaMIPSI-A to the jugular foramen without rerouting of the fallopian canal is highly valuable for selected tumors of the jugular foramen. It is less invasive than other skull base approaches, and it allows safe and complete tumor removal in appropriate patients.


Introduction
The jugular foramen is located deep at the posterolateral skull base in the posterior fossa. Tumors involving the jugular foramen have close relationships to the carotid artery, sigmoid sinus, jugular bulb, lower cranial nerves, fallopian canal, and the labyrinthine block. Jugular foramen tumors (JFTs) may originate from the jugular foramen itself (primary JFTs), or they may extend from adjacent structures into the jugular foramen (secondary JFTs). Due to the complex anatomy and their variable extensions, both primary and secondary JFTs present one of the most difficult lesions to access and resect surgically [4,26,41]. To facilitate selection of the most appropriate surgical approach for gross total resection, several grading systems for JFTs were developed based on tumor location, size, and extent [24,27,38]. Shin et al. described a modified Fisch classification (Table 1), categorizing JFTs as follows: type A, tumors limited to the middle ear; type B, tumors limited to the tympanomastoid area (without destruction of bone in the infralabyrinthine compartment); type C, tumors limited to the infralabyrinthine area; type D, tumors with intracranial extension; and type V, tumors involving the vertebral artery. Each group was further subdivided into subgroups to differentiate the intraosseous or intradural extension [50].
A variety of surgical approaches allowing posterolateral, superior, and anterolateral exposure of the jugular foramen has been described [5,7,13,14,18,25,31,44,48]. We have reported previously a morphometric anatomical study describing the surgical anatomy of a novel route to the jugular foramen -the navigated minimally invasive presigmoidal suprabulbar infralabyrinthine approach (NaMIPSI-A) without rerouting of the facial nerve [10]. Our morphometric cadaver study showed that this approach is suited for selected tumors including C1, De1, De2, Di1, and Di2 JFTs according to the modified Fisch classification. This approach has been used first in 2000 for resection of a De2 JFT by Krauss and Bergler in the frame of an interdisciplinary procedure (unpublished data).
The aim of the present study is to present our further experience with this approach in selected patients, to evaluate the degree of tumor resection, approach-related morbidity, and outcome.

Material and methods
Over a 15-year period, 5 patients with JFTs were selected for the NaMIPSI-A without rerouting of the facial nerve. Only Fisch class C and D tumors which were not deemed suitable for a classical suboccipital lateral approach were considered possible candidates. Also, patients with widespread infiltration of the petrous bone were excluded. The goal of the surgical procedure was gross total or near-total tumor resection with preservation of function in all cases.
The standard protocol included a computer tomography (CT) scan before and 6 h after surgery with bone window imaging. Before surgery, 3 months after surgery, and then at 1-year intervals, magnet resonance imaging (MRI) was obtained, and the neurological outcome was assessed.
The JFTs were classified according to the modified Fisch classification as described by Shin et al. [50] (Table 1).
While developed originally for primary tumors, it was adapted for secondary tumors in the present study. The extent of tumor resection was determined according to the intraoperative judgement of the surgeon and confirmed by the radiological examination after surgery. The extent of resection was graduated as (a) gross total resection (complete tumor resection) (GTR), (b) near total resection (remnants of less than 5% of tumor) (NTR), or (c) subtotal resection (more than 5% residual tumor) (STR). The extent of tumor resection, cranial nerve function, and approachrelated morbidity were evaluated.
The study was performed according to the regulations of the local ethical committee of Hannover Medical School.

Surgical technique
Surgery was performed according to the principles as outlined in our previous description of surgical anatomy [10]. The patient was positioned prone in a modified concorde position. The head of the patient was fixed in a Mayfield clamp and rotated to the opposite side until the mastoid bone was parallel to the floor. All surgical steps were performed guided by navigation of the skull base as described elsewhere ( Fig. 1) [20,36,37]. After the navigation system was set up, a retroauricular curvilinear C-shaped skin incision was performed. The skin flap was reflected anteriorly to visualize the zygomatic root, the mastoid body, the mastoid tip, the supramastoid crest, and the asterion while the external auditory canal was preserved. The approach was carried out under continuous electrophysiological monitoring of the lower cranial nerves (IX-XI), hypoglossal nerve, facial and cochlear nerve, and somatosensory evoked potentials.
The facial nerve was exposed at the mastoid tip. The superficial mastoid between the sigmoid sinus and the Tumors with intracranial extradural extension < 2 cm in diameter De2 Tumors with intracranial extradural extension > 2 cm in diameter Di1 Tumors with intracranial intradural extension < 2 cm in diameter Di2 Tumors with intracranial intradural extension > 2 cm in diameter Di3 Tumors with inoperable intradural extension Class V Tumors involving the vertebral artery medial osseous wall of the fallopian canal was removed under microscopic vision via a high-speed drill up to the presigmoidal dura preserving the sigmoid sinus and the fallopian canal. In cases with extradural extension of the JFT posterior to the jugular foramen, the dorsal surface of the tumor was localized by navigation, and the tumorrelated widening of the infralabyrinthine space was taken into account. Otherwise, the mastoid bone was drilled up to the osseous posterior semicircular canal and the jugular bulb guided by the navigation system to determine the site of the JFT superior to the jugular bulb. After resection of the JFT superior to the jugular bulb, the lower cranial nerves and the intraforaminal part of the JFT were identified by pressing gently on the jugular bulb. This step allowed both resection of tumor localized within and ventral to the jugular foramen while preserving the lower cranial nerves. Tumor-induced osseous widening of the petrosal bone ventral to the jugular foramen and navigated guidance eased identification of the vertical and horizontal portion of the carotid canal and the lower border of the cochlea. After resection of the extradural tumor, the presigmoidal dura was covered with human fibrinogen patch, and the bone defect was packed with fat and fibrin glue. The skin was closed in a multilayer fashion.

Patient characteristics and clinical presentation
The five patients (two women, three men) had a mean age of 57 years (range, 48-65 years) at the time of surgery (Table 2). Before surgery, patients suffered from hypoglossal palsy (2/5), impaired hearing (2/5), dizziness (2/5), facial palsy (House-Brackmann grade III) (1/5), hoarseness (1/5), and dysphagia (1/5). All patients were available for 1-year follow-up. The mean follow-up was 67.6 months (range, 12-119). Two patients were admitted primarily for surgery. One patient (patient 2, with an intracranial metastasis of a clear cell renal cell carcinoma) had already undergone radiation therapy and chemotherapy elsewhere, another patient (patient 3, with chondrosarcoma grade II at the jugular foramen) had undergone an unsuccessful attempt of tumor removal via a retrosigmoid inframeatal approach previously, and the third patient (patient 4) had had chordoma surgery of the paranasal sinuses followed by radiation therapy. The patient with chondrosarcoma grade II presented with an abducens nerve palsy, a facial nerve palsy (House and Brackmann grade III), tinnitus, facial paresthesia, and impaired hearing after the previous surgery.

Complications of surgery and neurological outcome
There was no mortality and no approach-related morbidity. In all cases, no new neurological deficits and no deterioration of the clinical status occurred postsurgically. Right after surgery and in the long-term follow-up improvement of hypoglossal palsy, dizziness, hoarseness, and dysphagia were noted (Table 2). One patient had a temporary CSF leak which was managed successfully after placement of a lumbar drainage.

Degree of tumor resection
Two JFTs were graded as C1, one was graded as De1, and the other two as De2. A GTR was possible in three instances, whereas NTR was achieved in the other two ( Table 2). During the follow-up period, tumor recurrence occurred in both cases of the NTR group, while no tumor recurrence was noted in patients of the GTR group. In both cases with NTR, the approach had provided sufficient access for a GTR. However, the tumor was strongly adherent to the lower cranial nerves after previous radiation therapy, and it was decided to leave a small tumor remnant to allow preservation of neurological function. Both patients died during the follow-up period unrelated to the tumor in the jugular foramen: patient 2 because of multiple abdominal metastasis of the clear cell renal cell carcinoma and patient 4 after repeated surgeries for recurrent chordoma of the paranasal sinuses.

Case 2
A 58-year-old man had an 11-year history of clear cell renal cell carcinoma of the right kidney treated by nephrectomy and followed by immunotherapy. He subsequently underwent resection of metastases of the spleen, pancreas, left groin, and osseous metastasis of the ribs and the scapula followed by chemotherapy. Years after the initial diagnosis, an asymptomatic tumor at the jugular foramen on the left side was detected, suggesting the diagnosis of metastasis. Radiation therapy was administered and for 4 years, no increase in tumor size and no neurological deficits occurred. Thereafter, the patient complained about intermittent hoarseness and dysphagia, hypoglossal palsy, and local pain at the mastoid bone on the left side. MRI and CT imaging showed an increase in tumor size (maximal diameter 35 × 40 × 35 mm). The tumor was classified as De2 according to the modified Fisch classification ( Fig. 2A and B). After admission, digital subtraction angiography showed a strongly vascularized tumor which was partially embolized. The tumor was resected via the NaMIPSI-A, and NTR was achieved by careful dissection of the tumor from cranial nerves IX and X within the jugular foramen. There were no postoperative complications, and both hoarseness and hypoglossal palsy improved during hospital stay. Postoperative CT confirmed NTR (Fig. 2c and d). Histologically, a metastasis of the clear cell renal cell carcinoma was confirmed. Adjuvant low-dose radiation therapy and chemotherapy was administered. During follow-up period, multiple abdominal metastases were noted, and a recurrence of the JFT. The patient died 7 months thereafter subsequent of the multiple abdominal metastases.

Case 3
A 65-year-old man presented with a 2-month history of dizziness and impaired hearing on the left side. There were no lower cranial nerve palsies. CT and MRI imaging showed an oval-shaped tumor on the left side (maximal diameter 24 × 19 × 21 mm) with poor contrast enhancement and osseous destruction ( Fig. 3a and b). The tumor was localized within the jugular foramen extending to the apex of the petrous bone, involving the vertical and horizontal petrous portion of the carotid canal. According to the modified Fisch classification, the tumor was classified as De1.
GTR via the NaMIPSI-A without rerouting of the facial nerve was performed. The osseous resection cavity was filled with fat and covered with fibrin glue. No postoperative complications were encountered. GTR of the tumor was verified on the postoperative cranial MRI and high-resolution CT ( Fig. 3c and d). Histology disclosed a cholesterol granuloma. During the postoperative course, dizziness subsided. Thirtyone months after tumor removal, a small contrast-enhancing structure at the apex of the petrous bone was seen on MRI imaging which did not increase in size on subsequent imaging, suggesting the diagnosis of scar tissue. Follow-up for a total of 119 months postsurgically was unremarkable.

Case 5
A 48-year-old woman presented with a 4-year history of dizziness, hearing loss, dysphagia, abducens nerve, and facial nerve palsy (House and Brackmann Grade III) on the left side after an unsuccessful attempt of previous surgery via a retrosigmoidal inframeatal approach. The cranial MRI and high-resolution CT showed an increase of tumor size (maximal diameters 20 × 10 × 12 mm) ( Fig. 4a and b). The tumor was classified as C1.
A GTR via the NaMIPSI-A was carried out. There were no postoperative complications. Postoperative cranial MRI and high-resolution CT confirmed GTR of the tumor (Fig. 4c and d). Histological examination revealed chondrosarcoma grade II and radiation therapy was initiated thereafter. During the follow-up period of 69 months, no tumor recurrence was noted on cranial MRI. Dysphagia and dizziness subsided postoperatively.

Discussion
Our present study demonstrates the feasibility of the NaMIPSI-A without rerouting of the facial nerve in patients with various tumors of the jugular foramen avoiding postoperative morbidity, in particular lower cranial nerve deficits. While some components of this approach have been described earlier [1,3], the novelty of our approach, however, is the stepwise development of its components aided by navigation.
In our previous morphometric anatomical study, we have shown that this approach may provide access for selected Fisch class C and D tumors [10]. We indicated that tumors destroying the osseous walls of the jugular foramen and jugular bulb with limited involvement of the vertical portion of the carotid canal but without infiltration or destruction of the anatomical structures around the infralabyrinthine space could be accessed through the presigmoid infralabyrinthine space via resection of the retrolabyrinthine petrous bone between the fallopian canal, the presigmoidal dura, the roof of the jugular bulb, and the inferior border of the posterior canal. By opening the presigmoidal dura, additional access can be obtained intradurally between the presigmoidal dura, the brainstem, the intradural part of the facial nerve, and the intradural part of the lower cranial nerves.
Here, we demonstrate that it allowed GTR in three patients, and NTR in two with marked tumor adherence to the lower cranial nerves after previous radiation therapy.
While neurological deterioration did not occur in any patient, neurological improvement was noted in 4 instances. Avoiding the sacrifice of important anatomical structures, sufficient access could be achieved in all selected tumors as determined by our previous study on surgical anatomy. Although all cases in the present study are secondary JFTs extending into the jugular foramen, the NaMIPSI-A is considered suitable as well for primary JFTs.
JFTs may originate from the jugular foramen itself, or they may extend from adjacent structures into the jugular foramen. Through the aperture of the jugular foramen, the tumors may grow in different directions. Thus, JFTs can have an intradural, intraforaminal-intradural, extradural, intraforaminal-extradural, or both extra-intradural location [8,9,27,44]. The choice of the appropriate surgical approach to JFTs should provide adequate access, minimal brain manipulation, minimal risk of approach-related morbidity, and safe GTR in a single stage. For achieving the goal of successful GTR with minimal risk of approach-related morbidity, it is important to expose only the necessary surrounding structures depending on the extension of the JFT. Additionally, technical advancements in microneurosurgery, neuroimaging, intraoperative monitoring, and the introduction of image-guided skull base surgery permit safer GTR of JFTs with considerable reduction of morbidity and mortality [33,51]. Depending on the location and extension of JFTs, several approaches have been described to gain sufficient access for radical tumor resection [6,26,28,42]. Related to the external auditory canal, all these approaches are grouped as posterior, lateral, or anterior approaches [10,18,26]. Also, several combinations of surgical routes have been described [5,18,30,40]. When discussing the different approaches in the following, one should be aware that in most studies, primary JFTs were treated, and that a direct comparison with our series including secondary JFTs cannot be made.
The suboccipital retrosigmoidal approach represents the most important and well-known standard posterior approach. The suboccipital retrosigmoidal approach is particularly suited for JFTs located intradurally. Access to intraforaminal and extradural parts of JFTs, however, is not possible like with the NaMIPSI-A [18, 26-28, 34, 44]. In an anatomical study, Matsushima et al. described a suprajugular extension of the subocciptal retrosigmoidal approach to JFTs [32]. They noted that suprajugular drilling of the area between internal acoustic meatus, roof of the jugular foramen, and anteromedial part of the endolymphatic depression permits removal of some JFTs located mainly in the cerebellopontine angle with intraforaminal extension and into the upper part of the jugular foramen. However, they emphasized that the retrosigmoidal suprajugular approach gains no access to the extradural part of JFTs. Samii et al. reported GTR of JFTs in 7 patients treated with an endoscopically assisted retrosigmoidal suprajugular approach [43]. They stressed the usefulness of this approach for tumors in the cerebellopontine angle with small extension into the jugular foramen. In a recent retrospective clinical study, Matsushima et al. reported 19 patients with JFTs mainly located intradurally with partial extension into the upper jugular foramen treated via a retrosigmoid suprajugular approach [33]. In 18 instances, GTR was possible without recurrence during the follow-up period. They indicated that JFTs located predominantly in the cerebellopontine angle extending into the upper part of the jugular foramen without invading the sigmoid-jugular venous system would be appropriate for removal via the retrosigmoidal suprabulbar approach. For JFTs extending more inferiorly or extending intra-and extracranially with intraforaminal invasion, they suggested not to use the retrosigmoidal suprajugular approach alone. Recently, Constanzo et al. also outlined the advantages, disadvantages, and indications of the retrosigmoidal suprajugular approach [12]. They advocated resection of JFTs mainly located intradurally with extension up to 10 mm into the jugular foramen via the retrosigmoidal suprajugular approach, while JFTs with extension to the anterior half of the jugular foramen were deemed as not suitable. Furthermore, they considered that drilling of the small suprajugular area, right above the lower cranial nerves and the sigmoid sinus, has an inherent risk of injuring the jugular bulb and the lower cranial nerves. We may suggest that in such cases, the retrosigmoidal approach could also be combined with the NaMIPSI-A in order to gain access for both JFTs.
Lateral approaches are favored usually by ENT surgeons. The most familiar lateral approaches are the infratemporal approach type A, the translabyrinthine-transcochlear approach, the petro-occipital approach, and the juxtacondylar approach. Commonly, lateral approaches gain access for resection of extradurally located JFTs. Resection of intradurally located JFTs with lateral approaches is limited. The infratemporal approach type A is one of the most familiar lateral approaches providing access to large extradurally located JFTs [14,24]. However, blind sack closure of the external auditory canal with removal of the middle ear causes hearing loss, and transposition of the facial nerve is associated with a risk of permanent peripheral facial nerve palsy [14,15,46]. The translabyrinthine-transcochlear approach allows only resection of extradural JFTs. Sacrificing the labyrinthine block, sacrificing the cochlea, and transposition of the facial nerve may result in vertigo, hearing loss, and persistent facial nerve palsy [2,21,22]. The petro-occipital approach is a combination of the retrolabyrinthine and retrosigmoidal approach. It is suitable for intradurally and extradurally located JFTs. While the petro-occipital approach allows preserving the external auditory canal, the middle ear, and the facial nerve, the sigmoid sinus is ligated. Ligation of the sigmoid sinus, however, may increase the risk of venous congestion [35,45]. The more recently described juxtacondylar approach gains a wide postero-inferior access to the extradural part of the jugular foramen [7,17]. The risk of facial nerve palsy and the risk of hearing loss are avoided by saving the labyrinthine block and the fallopian canal. However, removal of the occipital condyle represents a potential risk for craniocervical junction instability [7,11,17,49].
Anterior approaches alone are not preferred for JFTs as they allow access only to small ventrally located JFTs. The subtemporal-infratemporal approach represents the major variant of the anterior approaches. Frequently, the subtemporal-infratemporal approach is combined with lateral approaches for JFTs with extradural ventral extension [19,40]. Due to the permanent anterior transposition of the facial nerve, resection of the mandibular condyle, and resection of the tympanic part of the temporal bone, the subtemporalinfratemporal approach is often associated with hearing loss, facial palsy, and jaw malocclusion.
In JFTs extending mainly into the petrous bone without destruction of the important neurovascular and osseous anatomical structures, preserving important anatomical structures might reduce the approach-related morbidity. In such cases, the NaMIPSI-A may present a favorable alternative to the classical lateral approaches. If there is osseous destruction by the tumor in the infralabyrinthine space, the infralabyrinthine approach can be widened accordingly.
With regard to the technical progress in radiosurgery, some have recommended subtotal resection with minimal dissection of neurovascular structures in the jugular foramen to improve neurological outcome followed by radiation therapy of the tumor remnants to decrease the rate of recurrence [8,16,23,29,39]. Radiation therapy, however, may result in tumor adherence to neurovascular structures around the jugular foramen making repeat surgeries more difficult [47,52]. Repeat surgeries, in general increase the risk of lower cranial nerve injuries due to scarring. In such cases, only NTR may be possible, as also seen in two patients of the present study.
There is no consensus on the selection of the optimal surgical approach for JFTs. The choice of the approach depends mainly on the personal experience and preference of the surgeon. Appropriate patient selection and careful consideration of surgical anatomy are pivotal for applying the approach presented here. JFTs with limited intraforaminal and intradural extension without destruction of important neurovascular and osseous anatomical structures are considered to be suited best. If JFTs extend more inferiorly through the jugular foramen, are or located predominantly within the posterior fossa or occupy both intra-and extracranial spaces with intraforaminal invasion, this approach should not be selected for GTR. In such cases, the infralabyrinthine approach, however, may be combined with other approaches.

Conclusion
The NaMIPSI-A to the jugular foramen without rerouting of the facial nerve provides safe and sufficient access to resect selected JFTs. According to the modified Fisch classification, we recommend this approach for JFTs graded as C1, De1, and De2. Also, additionally opening of the presigmoidal dura may allow access to Di1 and circumscribed Di2 JFTs.