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Introduction
The inferior petrosal sinus (IPS) is an important paired structure in the posterior drainage system and the shortest route within the skull for draining venous blood from the cavernous sinus (CS) to the junction of the sigmoid sinus and superior jugular bulb [1-7]. The remnant of the fetal head sinus after it forms the sigmoid sinus, the pre-otic sinus, and proximal ventral myelencephalic vein contributes to the formation of the inferior petrosal sinus [3-8]. The conventional carotid vertebral angiogram/venogram has been an important tool for visualizing the IPS [5], which is important in other ways apart from venous blood drainage. In medical application it is used in bilateral sampling, which is valuable in combination with corticotropin-releasing hormone stimulation both for diagnosing Cushing’s disease and also for distinguishing it from ectopic adrenocorticotropic hormone (ACTH) levels [7-12]. Additionally, owing to its position and ease of access, the IPS is routinely used for transvenous embolization of cavernous sinus dural arteriovenous fistulas (CSDAVFs), even in cases when the IPS is radiologically occluded [6, 12-15].
The IPS runs within a bony channel called the inferior petrosal sinus groove (IPSG) [3, 16, 17]. Contributors to the IPSG include the wall of the petro-occipital fissure, the occipital bone, and the petrous portion of the temporal bone [6,18]. The IPS has been extensively studied using microsurgery, magnetic resonance imaging, and variations of computed tomography (CT) as well as angiography [5, 13, 18]. Although major studies have used angiography, Gebarski and Gebarski [18] pioneered an IPS imaging-anatomical correlation that specifically elucidated the morphology of the IPSG, its asymmetrical nature, and its variations. Additionally, a classification system for the IPS has been developed [8].
To our knowledge, while the IPS has been studied in detail, there has been no comparable in-depth study of the IPSG including its overall structure and variations. Doppman et al. [9] demonstrated the importance of the IPS for bilateral sampling. It has been suggested that the contribution of the IPSG to IPS anatomy could be a factor in the rare false-negative results from sampling, but this has yet to be studied. Also, in transvenous embolization of CS fistulas using the IPS, variations in IPS size determined the type of probe and catheter employed [6, 14].
Given the importance of the IPSG, this project serves as the first in-depth study of it. Thorough analysis led to the development of a classification scale to account for differences in the sulci within a skull and among multiple skulls. This classification scale can potentially inform various interventions for pathological states involving the IPS and skull base.
Materials and Methods
One hundred dry adult human skulls (200 sides) were studied in order to verify the presence of an IPSG at the skull base. The exact age and sex of the specimens were not known. The groove was defined as the bony indentation running from inferolateral to the dorsum sella medially and the apex of the petrous part of the temporal bone laterally, traveling inferiorly along the base of the petrous part of the temporal bone and medial to the jugular tubercle of the occipital bone and terminating at the anteromedial aspect of the jugular foramen. When magnification was necessary, a surgical microscope was used (Zeiss, Oberkochen, Germany). Measurements of these structures were made, and a classification developed to help better describe the anatomy of these structures. Measurements included the maximal width and depth of the IPSG. All measurements were performed using microcalipers (Mitutoyo, Kawasaki, Japan). Statistical analyses were performed (Student’s t-test) to discern any differences between sides with significance set at P<0.05. Correlation between morphological findings was analyzed using Pearson’s correlation coefficient.
Results
We identified an IPSG in the majority of specimens (Fig. 1). The IPSG began anteriorly where the apex of the petrous part of the temporal bone articulated with the sphenoid part of the clivus (crossed in life by Gruber’s ligament), traveled posteriorly, in a slight medial to lateral course, primarily just medial to the petro-occipital fissure, and ended at the anteromedial aspect of the jugular foramen. When the IPSGs were grouped into five types (Fig. 2):
Type I: No IPSG (20; 10.0%)
Type II: A partial IPSG (13; 6.5%)
Type III: A complete IPSG (160; 80.0%)
Type IV: A partial IPS tunnel (5; 2.5%)
Type V: A complete tunnel (2; 1.0%)
Partial and complete tunnels (i.e., type IV and type V IPSG) occurred medial to a protuberant part of the petrous part of the temporal bone and lateral to the jugular tubercle of the occipital bone (Fig. 3). This protuberant part of the bone (Fig. 2) was approximately one centimeter wide and extended medially toward the jugular tubercle of the occipital bone and thereby allowed the more lateral part of the IPSG to travel inferior to it when a type IV and converted the IPSG into a tunnel when a type V. One type III IPSG (left side) was related to a jugular foramen that was completely divided by a bony separation (Fig. 4). Therefore, the IPSG connected to the more anterior part of this split jugular foramen. Complete IPSGs were more common on right sides (P<0.05). The mean depth of the IPSG was 1.9 mm (0.75–3.2 mm) and the mean width of the grooves was 3.4 (2.1–5.6 mm). The mean length of the IPSG was 25 mm (range 20–28.5 mm). Larger grooves were moderately correlated (r=0.65) to a more prominent jugular tubercle and were more commonly (70%) located on right sides (P<0.05). Larger jugular tubercles were strongly correlated (P=0.70) to the presence of a partial or complete tunnel i.e., types IV and V. An asymmetrical IPSG was common on left and right sides of the same specimen (Figs. 5, 6). No gross pathology of the skull base was identified in any specimen.
Discussion
We identified an IPSG in the majority of specimens. Although some [19] have stated that the IPS overlies the petro-occipital fissure, our findings demonstrated that the IPSG was mostly lateral to this skull base joint. The anatomical-imaging correlation, more specifically axial CT images, by Gebarski and Gebarski [18] revealed a relationship between the size of the IPS and the IPSG (Fig. 6). Their results showed that the deeper the IPSG, the larger the IPS. This conclusion was inferred from results correlating 40 CT studies. Therefore, if a type III IPSG as classified herein is identified on preoperative or preprocedural imaging, a larger IPS should be anticipated. Types IV and V (incomplete and complete tunnels), when present (2.5% and 1.0%, respectively) were compressive in nature as the dimensions of the pathway for the IPS were less than sides without a tunnel or partial tunnel. Therefore, patients with these types of grooves would be expected to have a small sinus at this location.
Petrosal sinus sampling is a mainstay for diagnosing Cushing syndrome, and for distinguishing this condition from ectopic ACTH levels in the brain with almost 100% sensitivity [7-12]. Prior to the study by Doppman et al. [9], false-negative rates for this diagnostic method were as low as 5%. A false negative led to delays in transsphenoidal surgery. Sonography revealed a hypoplastic IPS or a plexiform IPS on the microadenoma side compared to the ipsilateral region, contributing to alteration of the venous channels [9]. Our observations of IPSG indicate how its variations in width or depth can lead to an atrophic sinus, implying other possible reasons for false negatives in petrosal sampling for Cushing’s disease. Additionally, if these grooves are tunnel in configuration (e.g., types IV and V), microcatheters placed into these patients might meet resistance.
Transvenous embolization for CSDAVFs is reportedly preferred because it gives better outcomes and it is the gold standard for this condition [6, 12-15]. The many other venous routes to the CS include the superior petrosal, facial, and superior ophthalmic veins, but the IPS remains the mainstay for transvenous embolization regardless of whether the condition in the CS is ipsilateral or contralateral, and even when the IPS is occluded [6]. Jia et al. reported some failure in the performance of transvenous embolization through a thrombosed IPS, which necessitated a switch from the micro guidewire to a 0.035-inch guidewire [6]. From our results, an in-depth knowledge of the IPSG and how it affects access to the IPS can help in similar interventions in the future. For example, as with IPS sampling, if these grooves are tunnel in configuration (e.g., types IV and V), guidewires placed into these patients might meet resistance. Furthermore, the IPSG classification scale can serve in modifying the current guidewires to produce newer guidewires with an expanded scale to meet the highlighted variations and to facilitate penetration of the IPS.
As we identified an IPSG in the majority of specimens, as mentioned above, 10% of sides did not have an identifiable IPSG. This is due to either the absence of the IPS or a deviation in its course. Absence of the IPS has been reported at approximately 1% of the population [11]. As an osteological study, we could not verify the course of the IPS but this might imply a variant inferior course or size of the sinus. Shiu et al. [20] have classified IPS variations from the venography of 53 patients, these authors identified four distinct patterns of drainage into the inernal jugular vein (IJV) as follows (Fig. 7):
Type I (45% of patients): The most common version where the IPS drains directly in to the IJV
Type II (24% of patients): In these cases, the IPS drained into a communicating vein that united the internal jugular bulb with the deep cervical plexus
Type III (24% of patients): In type III variants, the IPS exists essentially as a plexus of veins. The cavernous sinus drains into various locations via this plexus
Type IV (7% of patients): The IPS, in these cases, is well formed. However, instead of draining into the superior jugular bulb, it drains into the deep cervical plexus of veins
Lastly, we found that an enlarged jugular tubercle correlated to a larger IPSG. Surgically, this relationship would be important as large tubercles are often drilled down for better access to, for example, vertebrobasilar or posterior inferior cerebellar artery aneurysms via a far lateral transcondylar approach [21]. As our study found partial and complete tunnels (i.e., type IV and type V IPSG) medial to a protuberant part of the petrous part of the temporal bone (we suggest terming this the petrous ala) and lateral to the jugular tubercle of the occipital bone, skull base surgeons performing such maneuvers e.g., drilling of the jugular tubercle should be cognizant of the potential for an enlarged IPS in such situations. This relationship could also help predict larger IPS on imaging.
An improved knowledge of the bony pathways that the intracranial dural venous sinuses take as they exit the cranium is clinically useful. Radiological interpretation of such bony landmarks might improve patient diagnoses and surgically, such anatomy could decrease patient morbidity during approaches to the posterior cranial fossa. Based on our study, complete IPSGs were more common on right sides and larger grooves were moderately correlated to a more prominent jugular tubercle and were more commonly located on right sides. Larger jugular tubercles were strongly correlated to the presence of a partial or complete tunnel. To our knowledge, bony tunnels for the IPS have not previously been described.
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