Simplifying the Surgical Classification and Approach to the Posterolateral Skull Base and Jugular Foramen Using Anatomical Triangles

Introduction Lesions of the jugular foramen (JF) and postero-lateral skull base are difficult to expose and exhibit complex neurovascular relationships. Given their rarity and the increasing use of radiosurgery, neurosurgeons are becoming less experienced with their surgical management. Anatomical factors are crucial in designing the approach to achieve a maximal safe resection. Methods and methods Six cadaveric heads (12 sides) were dissected via combined post-auricular infralabyrinthine and distal transcervical approach with additional anterior transstyloid and posterior far lateral exposures. Contiguous surgical triangles were measured, and contents were analyzed. Thirty-one patients (32 lesions) were treated surgically between 2000 and 2016 through different variations of the retro-auricular distal cervical transtemporal approaches. Results We anatomically reviewed the carotid, stylodigastric, jugular, condylar, suboccipital, deep condylar, mastoid, suprajugular, suprahypoglossal (infrajugular), and infrahypoglossal triangles. Tumors included glomus jugulare, lower cranial nerve schwannomas or neurofibromas, meningiomas, chondrosarcoma, adenocystic carcinoma, plasmacytoma of the occipitocervical joint, and a sarcoid lesion. We classified tumors into extracranial, intradural, intraosseous, and dumbbell-shaped, and analyzed the approach selection for each. Conclusion Jugular foramen and posterolateral skull base lesions can be safely resected through a retro-auricular distal cervical lateral skull base approach, which is customizable to anatomical location and tumor extension by tailoring the involved osteo-muscular triangles.


Introduction
Surgical access to distal cervical and jugular foramen (JF) lesions is difficult given the anatomical complexity of the region, technical challenges, and risk of neurovascular injuries. Approach selection is key in devising the surgical strategy and achieving complete resection. Given the usual depth of the pathology, muscular and bony structures should be unlocked in a stepwise and targeted fashion. Tailoring the approach to the individual case allows for adequate exposure around the lesion while minimizing unnecessary steps, wasted time, and risk of collateral injuries.
Tumor extension has been classified based on pathological diagnosis and its anatomical extension (glomus tumors, cranial nerve schwannomas, meningiomas) [1][2][3][4][5][6][7]. Several classification schemes have also been proposed to help plan the surgical approach. Dr. Albert Rhoton Jr. classified the JF approaches into an anterior group through the tympanic bone (preauricular subtemporal-infratemporal fossa approach), a lateral group through the mastoid bone (post-auricular transtemporal infralabyrinthine approach, and other transmastoid approaches), and a posterior group (retrosigmoid, far lateral and trans-condylar approaches) [8]. The senior author (JHR) traditionally adopted the lateral distal cervical retro-auricular transtemporal (LDC-RATT) approach because it offers direct access to the JF, is versatile, and can be tailored to individual lesions [9,10]. We recently deconstructed this approach into anatomical triangles and analyzed its different 1 angles of exposure [11].
In this paper, we review a clinical series of 32 lesions where a modification of the LDC-RATT was used by the senior author (JHR) for surgical resection of distal cervical and posterolateral skull base lesions, either extending to or in close proximity to the jugular foramen. We classified these according to their anatomical extension and analyzed the anatomical factors influencing approach selection and modification. Such a classification was combined with an illustration of the jugular foramen triangles in planning and executing the approach.

Anatomical dissections
Six preserved cadaveric heads (12 sides) were dissected at the Medical Education and Research Institute (MERI) microsurgical laboratory in Memphis, TN. The heads had no known intracranial or cervical pathology and were fixed and injected with colored silicone rubber. All cadaver specimens had preserved distal necks proximally, at least to the level of the omohyoid muscle.
Two types of retro-auricular curvilinear C-shaped skin incisions were made posterior to the pinna: either 3 cm posterior to the pinna for a standard lateral approach, or further medially close to the midline in order to expose the occipital condyle (modified approach with a far lateral component; Figure 1). Three major landmarks were constantly recognized: the mastoid tip, styloid process, and transverse process of the atlas (TP-C1). The following superficial triangles were defined and identified as previously described (Figures 2  and 3): (i) mastoid triangle, between the asterion, mastoid tip, and the supra-meatal crest ( Figure 2A) [12]; (ii) carotid triangle, limited by the omohyoid, the sternocleidomastoid (SCM), and the digastric muscles ( Figure  2B) [13]; and (iii) stylodigastric triangle between the digastric and the stylo-hyoid muscles ( Figure 2C) [12]. To expose the jugular foramen (blue), the approach unlocks the carotid, stylo-digastric, jugular, and mastoid triangles. A modified postero-lateral approach (red) extends the exposure medially to the condylar region, leading to the condylar, deep condylar, suboccipital, supra-hypoglossal, and infra-hypoglossal triangles. (A) Mastoid triangle: drilled between the supra-mastoid crest (SMC), asterion (label A), and mastoid tip (MT). It can be divided into an infra-labyrinthine or supra-jugular sector (red), and a pre-sigmoid sector (yellow  The atlanto-occipital joint (or occipitocervical joint, OCJ) is seen after mobilizing and retracting the vertebral artery (VA) inferiorly. (C) Supra-hypoglossal (yellow) and infra-hypoglossal (green) triangles: delineated after drilling the occipital condyle with the former leading to the infrajugular area, and the latter to the occipitocervical joint. Labels: aSMF: artery of stylomastoid foramen; CN-7: facial nerve; CN-12: hypoglossal nerve; JF: jugular foramen.
Detaching the digastric muscle and mobilizing it inferiorly exposed the TP-C1 and the surrounding deep muscular triangles: (iv) suboccipital triangle between the superior and inferior oblique muscles ( Figure 3A) [14], and (v) condylar triangle between the superior oblique and rectus capitis lateralis muscles ( Figure 3A) [15]. We also previously defined the (vi) "jugular triangle" between rectus capitis lateralis, TP-C1, and the base of the styloid process, as the lateral limit to the jugular foramen ( Figure 3A) [11]. We proposed the (vii) "deep condylar triangle" between the condylar emissary vein, the jugular process of the occipital bone (site of insertion of rectus capitis lateralis), and the transverse process of the atlas ( Figure 3B) [11]. This helped us delineate exactly where the occipital condyle is located from a lateral perspective. Drilling the occipital condyle led us to the hypoglossal canal. Above it, the (viii) supra-hypoglossal triangle was defined between the hypoglossal dura inferiorly, foramen magnum dura medially, and jugular bulb laterally. Below it, the (9) infra-hypoglossal triangle was identified between the hypoglossal dura, atlanto-occipital joint, and jugular foramen ( Figure 3C) [16].

Case series
We retrospectively reviewed illustrative cases in which different modifications of the LDC-RATT approach were used by the senior author (JHR) at our institution between 2000 and 2016. Emphasis was placed on challenging lesions, such as glomus jugulare tumors, lower cranial nerve schwannomas, jugular foramen meningiomas, and occipital condyle and/or atlanto-occipital joint lesions extending to the jugular foramen.
Pre-operative imaging (including computed tomography [CT] scans, magnetic resonance imaging [MRI], and, if available, four-vessel angiography) and intraoperative findings were reviewed on 31 patients treated surgically for 32 such lesions. We focused on the anatomical factors of these lesions, which were deemed crucial in planning the surgical approach. We obtained Institutional Review Board approval from The University of Tennessee Health Science Center (UTHSC) (No. 20-07874-XP). Informed consent was waived because of the retrospective nature of the data.
Anatomically, lesions were classified according to their origin and extension ( Table 1). Extracranial tumors (type 1) are limited to the distal cervical region. While type 1A lesions are located below the digastric muscle in the carotid triangle ( Figures 2B and 4), type 1B tumors are in the stylodigastric triangle close to the skull base ( Figures 2C and 5). Type 2 tumors are intracranial and involve at least the cerebello-medullary and/or the cerebello-pontine cisterns ( Figure 6). Type 3 tumors are typically located at the level of the skull base and are termed intra-osseous or intraforaminal. Type 3A is limited to the jugular foramen (Figure 7), while type 3B lesions extend to the petrous bone and/or the internal auditory meatus, and type 3C tumors to the occipital condyle region ( Figure 8A-8B). Type 4 tumors are dumbbell-shaped, with 4A involving the jugular foramen and 4B the medial aspect of the jugular foramen and hypoglossal canal ( Figure 9A-9B    Coronal T1 gadolinium-enhanced (A) and computed tomographic scan (B) of a mostly intradural glossopharyngeal schwannoma (case 8). The patient in their late 30s presented with hearing loss, tinnitus, and vertigo, and the tumor was mostly intracranial impinging toward the jugular foramen (type 2). A retroauricular incision was planned (C) and the mastoid triangle was exposed in both its presigmoid and suprajugular sectors (D). A combined presigmoid and retrosigmoid intradural approach was performed (E) to achieve a gross total resection, as seen on the postoperative coronal MRI scan (F). Labels: JB: jugular bulb; L: labyrinth; SS: sigmoid sinus.

FIGURE 7: Glomus jugulare tumor accessed via jugular triangle.
Exposure of the deeper surgical triangles, including the jugular triangle. (A) Axial T1 MRI scan demonstrating a left glomus jugulare tumor in a patient in their mid-40s presenting with hearing loss and pulsatile tinnitus (case 9). A lateral distal cervical retro-auricular transtemporal (infra-labyrinthine) approach was performed to expose the jugular foramen (JF) (B). The fallopian canal was skeletonized keeping a bone shell around the facial nerve (CN-7) to preserve it. After ligating the sigmoid sinus and the jugular vein, the vein was opened, and the tumor resected from within (C). The medial wall of the vein was preserved to protect the neighboring lower cranial nerves. Labels: CN-7: facial nerve; IJV: internal jugular vein; JF: jugular foramen; L: labyrinth; RCL: rectus capitis lateralis; SS: sigmoid sinus.  We then analyzed the different modifications of the LDC-RATT approach as employed in clinical practice by the senior author (JHR), compared to our anatomical dissections and of the described surgical triangles.

Anatomical dissections
Contents of the different triangles along with their respective measurements have been previously reported [11]. Table 2 summarizes the triangles as they relate to the modifications of the LDC-RATT approach, including the different possible surgical steps and exposure advantages related to the jugular foramen region.   Figures 2B, 2C, 4, and 5).
Both the digastric and SCM muscles attach to the mastoid bone and should be reflected if further steps of the approach are necessary. Drilling the mastoid bone can be compartmentalized into an infralabyrinthine space (or "suprajugular space" to expose the superior aspect of the jugular foramen and jugular bulb), and a retrolabyrinthine/translabyrinthine space (leading to the presigmoid dura; Figures 2A and 6). The IJV enters the JF in the jugular triangle (TPC1-rectus capitis lateralis-base of the styloid process). Thus, exposing a standard glomus jugulare tumor requires opening the carotid, stylodigastric, mastoid, and jugular triangles ( Figures 3A and 7). Palpating the transverse process of the atlas, the styloid process, and the mastoid tip is helpful in orienting the surgeon toward the correct triangles.
A modified LDC-RATT is helpful for lesions involving the region of the occipital condyle and medial aspect of the jugular foramen. This approach adds a far lateral exposure and is devised by curving the retro-auricular incision further medially. It allows the exposure of the occipital bone beyond the occipitomastoid suture and the suboccipital triangle beneath it. Again, the transverse process of the atlas represents a key anatomical structure that helps delineate the suboccipital triangle (where the vertebral artery is identified), and the condylar triangle (harboring the occipital condyle [OC]). The OC is delineated exactly in the deep condylar triangle, and drilling it exposes the hypoglossal canal. The supra-hypoglossal triangle aids in exposing the inferior aspect of the jugular foramen (described in the literature as the infrajugular approach), while the infra-hypoglossal triangle leads to the atlanto-occipital joint ( Figures 3B, 3C, and 8).

Case series
The confirmed pathological diagnosis of the reviewed lesions included: 13 lower cranial nerve schwannomas or neurofibromas (eight hypoglossal, two vagal, two glossopharyngeal, and one accessory), seven glomus jugulare/vagale tumors, seven meningiomas (mostly petrous or petroclival extending into the jugular foramen), one chondrosarcoma, one adenocystic carcinoma, one plasmacytoma of the occipitocervical joint, one eagle syndrome (hypertrophied styloid process compressing the internal carotid artery and causing transient ischemic attack [TIA] like syndrome), and one sarcoid lesion in the occipital condyle/medial jugular foramen area. Table 3 summarizes the clinical presentation, pathology, employed surgical approach, and extent of resection in each of these cases.   Type 1A tumors were approached through the carotid triangle. For more distal lesions beyond the angle of the jaw or the digastric muscle (type 1B), the stylodigastric triangle was opened by either mobilizing or detaching the digastric muscle ( Figures 2B, 2C, 4, and 8). Intradural tumors (type 2) were mostly located intracranially with limited intraforaminal extension. These were approached through the presigmoid, retrosigmoid, or lateral suboccipital (or far lateral) corridors (Figures 2A and 6). Intraosseous tumors (type 3) were located in the skull base (jugular foramen, occipital condyle, lower part of the mastoid, and petrous bone). These were accessed through the jugular triangle using a classic LDC-RATT approach if the origin of the tumor was believed to be in the jugular foramen (type 3A ; Figures 2d and 7). Extension along the petrous bone or to the petroclival area (type 3B) dictated a petrosal component to the approach (retrolabyrinthine, translabyrinthine, or a transcochlear approach). A modified LDC-RATT or a far lateral approach with a medially oriented incision, leading to the condylar triangles, was performed whenever the occipital condyle and medial aspect of the jugular foramen were compromised (type 3C ; Figures 3c, 8a, and 8b).

Case Presentation
Dumbbell-shaped tumors (type 4) required either combined or staged procedures through variations of the retro-auricular approach (Figures 2b and 4). A translabyrinthine, transcochlear, or retrosigmoid part was added to the LDC-RATT approach for type 4Ai tumors to further address the intracranial disease. Stereotactic radiosurgery was helpful to control the foraminal component after either removing the symptomatic intracranial (4Ai) or distal cervical parts (4Ae) in other cases.
True jugular dumbbell-shaped tumors (type 4At, comprising all intracranial, foraminal, and extracranial compartments) were treated with a staged distal cervical followed by retrosigmoid resection, or a combined LDC-RATT and translabyrinthine approach. Type 4B tumors (extending to the condylar triangle) were treated with a modified LDC-RATT approach combined with either a suboccipital retrosigmoid or an intradural far lateral approach (Figures 4 and 8).
In summary, important anatomical factors found to be highly influential on selecting the surgical approach included the following: displacement of the distal cervical internal carotid artery (if the tumor moved the artery anteriorly, this dictated a posterolateral, rather than anterior, approach); involvement of the occipital condyle; tumor extension to the petrous bone or to the internal auditory meatus; tumor vascularity and origin of arterial feeders; patency of the sigmoid sinus; and preoperative cranial nerve deficits (described in the Discussion section).
Given the overlap in surgical approaches and anatomical extensions, we combined previous classifications to help systematize posterolateral skull base and distal cervical lesions, regardless of their pathological diagnosis, in one scheme. Most of these lesions can be simplified into extracranial, intracranial, intraosseous/intraforaminal (at the level of the skull base), and dumbbell-shaped. We believe that this is helpful to tailor the surgical approach and its steps to each lesion and avoid the risks of radical exposures if not necessary.
On the other hand, Fisch divided the post-auricular approach itself into types A, B, and C based on the required anterior exposure. In the classic type A approach, a distal cervical dissection is combined with a radical mastoidectomy, with further transposition of the facial nerve to expose the posterior aspect of the infratemporal fossa and petrous carotid. While the type B approach extends to the petrous apex and clivus, type C widens the exposure to include the anterior aspect of the middle fossa and infratemporal fossa [17].
The post-auricular approach described by Fisch falls in the lateral group of approaches as classified by Rhoton (post-auricular transtemporal infralabyrinthine approach, and other transmastoid approaches) ( Figure 10A) [8]. However, it is more extensive and includes radical steps associated with a higher rate of complications, such as facial nerve transposition. The lateral approach (i.e., LDC-RATT) is versatile and can be customized to the specific anatomical location of the lesion ( Figure 10B) [11]. The styloid process may be removed to gain part of the exposure obtained from a preauricular subtemporal-infratemporal fossa approach (anterior group) [8,18]. The rectus capitis lateralis can be detached and the jugular process of the occipital bone drilled, overlapping with the precondylar variation of the far lateral approach (posterior group) [19]. In a modified LDC-RATT approach, the exposure is combined with a far lateral approach to access the condylar area [20].
To this end, we deconstructed the approach into sequential steps in predictable anatomical triangles ( Table  2 and Figure 1). In a similar way with cavernous sinus and middle fossa triangles, these can help compartmentalize the lesion and the operative stages required to reach it. Given the preponderance of radiosurgery and the rarity of these lesions, younger neurosurgeons are becoming less familiar with the subtle nuances of approaching jugular foramen pathologies. Lesions are sometimes deemed inoperable or inaccessible given a poor approach selection. Although not necessary, the triangles can provide young neurosurgeons who are not familiar with the anatomy, with a diagrammatic tool until more intuitive knowledge is developed.
Besides the anatomical relationship with described surgical triangles, several anatomical factors were found to be crucial in deciding the surgical approach. If the internal carotid artery is displaced posteriorly, then an anterior jugular foramen approach needs to be considered, such as opening the stylodigastric triangle and resecting the styloid process ( Figures 2C and 5). However, if the tumor is further anterior in the infratemporal fossa, then a pre-auricular infratemporal fossa approach should be undertaken [18].
Involvement of the occipital condyle and the hypoglossal canal is key in deciding on the medial extent of the approach (Figures 3B, 3C, and 9). In such instances, and even if the tumor originates in the jugular foramen, exposure is carried medially to the transverse process of the atlas in order to allow visualization of the superficial and deep condylar triangles. If the tumor originates more medially toward the foramen magnum, then a more medial approach may be selected (suboccipital or far lateral approach) [14].
Mastoid bone involvement can be divided into two major sectors: infralabyrinthine (or suprajugular) space and a presigmoid sector (retrolabyrinthine, translabyrinthine, and transcochlear approaches) [16]. An infralabyrinthine mastoidectomy usually allows good exposure of the jugular foramen and its superior aspect (Figures 2A and 6). If the tumor extends to the petrous bone and petrous ICA, then a petrosal approach should be added to the operative plan [12].
Tumor vascularization should be analyzed in a pre-operative angiographic study. Branches of the ECA (occipital, ascending pharyngeal, posterior auricular, and stylomastoid foramen arteries), can be exposed in the distal carotid and stylodigastric triangles ( Figure 4C). Meningeal and muscular branches of the vertebral artery can be exposed in the suboccipital and condylar triangles. Studying venous anatomy is also mandatory. The sigmoid sinus may be already occluded, and it may be possible to ligate and open it ( Figures  3A and 7). The insertion of vein of Labbé should be scrutinized to decide the best area in which to perform such a ligation proximally (distal to Labbé) [9]. Venous collaterals may be enlarged and may constitute a major source of bleeding (e.g., vertebral plexus, condylar emissary vein).
Pre-operative cranial nerve deficits can dictate a more aggressive surgical approach, such as a translabyrinthine or transcochlear approach in patients with complete hearing loss (e.g., cases 13, 14, and 18); facial nerve transposition in patients with severe facial palsy; more radical resection along the lower cranial nerves in patients with vocal cord paralysis and who already underwent a tracheostomy and/or a gastrostomy tube insertion procedure (e.g., cases 17 and 18). Multidisciplinary postoperative rehabilitation of cranial nerve deficits should be anticipated and started as soon as possible to optimize the chances of long-term recovery.

Conclusions
Despite their difficulty, lesions located in the distal cervical and postero-lateral skull base (jugular foramen and peri-condylar) regions continue to require surgical interventions in the era of stereotactic radiation. The mainstay of surgical treatment is the selection and implementation of the appropriate approach, providing adequate access without unnecessary, or even risky, dissections. Customizing the approach is simplified using anatomical compartments or triangles, which can be predicted on pre-operative imaging and unlocked in a stepwise fashion. These include the carotid and stylo-digastric triangles in the cervical region, the mastoid triangle, the jugular, condylar and sub-occipital triangles under the digastric muscle, and the deep condylar, supra-hypoglossal, and infra-hypoglossal triangles in the condylar region. The lateral distal cervical retro-auricular trans-mastoid approach is versatile and can be minimized, adjusted, or extended in each case. We provide an anatomical classification and a surgical roadmap to help young neurosurgeons plan these surgeries based on part of the senior author's (Jon H. Robertson) experience.

Additional Information Disclosures
Review Board approval was provided by The University of Tennessee Health Science Center (No. 20-07874-XP). Consent was waived because of the retrospective nature of the data. . Animal subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.