Surgical Treatment of Selected Tumors via the Navigated Minimally Invasive Presigmoidal Suprabulbar Infralabyrinthine Approach without Rerouting of the Facial Nerve

DOI: https://doi.org/10.21203/rs.3.rs-1325294/v1

Abstract

BACKROUND: The feasibility of a novel skull base approach, the navigated minimal ly 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.

OBJECTIVE: Here, we present our clinical experience with this approach for selected JFTs, with a particular focus on its efficacy and safety.

METHODS: 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.

RESULTS: Five patients (two women, three men; mean age 57y, 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.

CONCLUSIONS: 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 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, labyrinthine block and cochlea. Due to the complex anatomy and their variable extensions, jugular foramen tumors (JFTs) present one of the most difficult lesions to access and resect surgically. [2,24,38] 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. [22,25,35] 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. [47]

A variety of surgical approaches allowing posterolateral, superior and anterolateral exposure of the jugular foramen has been described. [3,5,11,12,16,23,41,45]We have reported previously a morphometric anatomical study describing the surgical anatomy of a novel route to the jugular foramen, the NaMIPSI-A without rerouting of the facial nerve. [8] 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 had been used first for resection of a De2 JFT by Krauss and Berger in the frame of an interdisciplinary procedure.

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 treated via the NaMIPSI-A without rerouting of the facial nerve. 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 six hours after surgery with bone window imaging. Before surgery, three months after surgery and then at one-year intervals magnet resonance imaging (MRI) was obtained and the neurological outcome was assessed.

The JFTs were classified neuroradiologically according to the modified Fisch classification as described by Shin et al. [47] (Table 1). 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 approach-related 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. [8] 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). [18,33,34] After the Medtronic navigation system was set up (Stealth Station, Medtronic), 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 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 tumor-related 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 Tachosil®, and the bone defect was packed with fat and fibrin glue. The skin was closed in a multilayer fashion.

Results

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 chrondrosarcoma grade II presented with a 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 longterm 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.

Illustrative cases

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 four 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 x 40 x 35 mm). The tumor was classified as De2 according to the modified Fisch classification (Figure 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 metastases 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 seven 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 x 19 x 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 cholesterolgranuloma. 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 x 10 x 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. In our previous morphometric anatomical study, we have shown that this approach provided adequate access for tumor removal of Fisch grade C1, De1, De2, Di1 and Di2 JFTs. [8] 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.

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. [6,7,25,41] The choice of the appropriate surgical approach to JFTs should provide adequate access, minimal brain manipulation, minimal risk of approach-related morbidity and safe gross total resection in a single-stage. For achieving the goal of successful gross total resection 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. [30,48] Depending on the location and extension of JFTs, several approaches have been described to gain sufficient access for radical tumor resection. [4,24,26,39] Related to the external auditory canal, all these approaches are grouped as posterior, lateral or anterior approaches. [8,16,24] Also, several combinations of surgical routes have been described. [3,16,28,37]

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. [16,24–26,31,41] In an anatomical study, Matsushima et al. described a suprajugular extension of the subocciptal retrosigmoidal approach to JFTs. [29] 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. [40] 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. [30] 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. [10] 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 increases the 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. [12,22] 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. [12,13,43] 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. [1,19,20] 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. [32,42] The more recently described juxtacondylar approach gains a wide postero-inferior access to the extradural part of the jugular foramen. [5,15] The risk of facial nerve palsy and the risk of hearing loss is avoided by saving the labyrinthine block and the fallopian canal. However, removal of the occipital condyle represents a potential risk for craniocervical junction instability. [5,9,15,46]

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. [17,37] 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 subtemporal-infratemporal 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. [6,14,21,27,36] Radiation therapy, however, may result in tumor adherence to neurovascular structures around the jugular foramen making repeat surgeries more difficult. [44,49] 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 is 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.

Declarations

Funding 

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Conflicts of interest 

The authors declare that they have no conflict of interest.

Competing Interests 

The authors have no relevant financial or non-financial interests to disclose.

Authors' contributions 

Zafer Cinibulak: Planning, data collection, designing, writing, literature survey, submission Shadi Al-Afif: Planning, designing, literature survey Makoto Nakamura: Planning, designing, literature survey, correction Joachim K. Krauss: Planning, designing, writing, literature survey, correction

Ethics approval 

The study was performed according to the regulations of the local ethical committee of Hannover Medical School.

Ackowledgements 

Not applicable.

Availability of data and materials 

Not applicable.

Code availability 

Not applicable.

Disclosure 

The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

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Tables

Table 1

Modified Fisch classification for jugular foramen tumors according to Shin et al. (2012)

Modified Fisch classification for jugular foramen tumors according to Shin et al. (2012)

 

Class A

 

 

Tumors limited to the middle ear

 

Class B

 

 

Tumors limited to the tympanomastoid area without destroying bone of the infralabyrinthine compartment of the temporal bone

 

Class C

 

Tumors extending, destroying bone of the infralabyrinthine and apical compartment of the temporal bone and involving the carotid canal

C1

Tumors with limited involvement of the vertical portion of the carotid canal

C2

Tumors invading the vertical portion of the carotid canal

C3

Tumors invading the horizontal portion of the carotid artery

C4

 

Tumors with extension to the foramen lacerum

 

 

Class D

Tumors with intracranial extension

De1

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


Table 2

Summary of demographic and clinical data

 

Neurological symptoms

 

Patient

Age, sex

Side

Tumor size

(mm)

Fish 

classification

Degree of 

tumor resection

Histopathology

Presurgical

Postsurgical

Follow-up 

(months)

 

1

 

63, M

R

19 x 12 x 22

C1

GTR

Benign fibrose lesion

Impaired hearing

Unchanged

117

 

2

 

58, M

L

35 x 40 x 35

De2

NTR

Metastasis of a clear 

cell renal cell carcinoma

Hoarseness

Hypoglossal palsy

Hoarseness -> improved Hypoglossal palsy -> improved

21

 

3

 

65, M

L

24 x 19 x 21

De1

GTR

Cholesterol granuloma

Dizziness

Impaired hearing

Dizziness -> improved

 

119

 

4

 

53, F

L

21 x 24 x 24

De2

NTR

Chordoma

Hypoglossal palsy

Hypoglossal palsy -> improved

12

5

48, F

L

20 x 10 x 12

C1

GTR

Chondrosarcoma grade II

Diplopia

Facial palsy HB III 

Facial paresthesia

 Dysphagia

Dizziness

Diplopia

Facial palsy HB III 

Facial paresthesia

Dysphagia -> improved 

Dizziness -> improved

69


M, male; F, female;  HB, House Brackmann; GTR, gross total resection; NTR, near total resection