An atypical anatomical variation of the petrosphenoidal ligament in a newborn cadaver

To report an atypical anatomical variation of the petrosphenoidal ligament in a newborn cadaver and to discuss its clinical significance. During a study of ten newborn cadavers, the skull base was dissected to reveal the anatomy of the petrosphenoidal ligament and its relationship with the abducens nerve. An atypical anatomical variation was observed, and this is described. The length of the right and left ligaments to the point where it splits into two arms, the joint length of the two ligaments at the junction of the clivus, the length of the ligament proceeding to the posterior clinoid process, and the abducens nerve’s diameter as it passes below the ligament were measured on ImageJ software. The petrosphenoidal ligaments were y-shaped, and the attachment of the proximal ligaments was bifid. In the midline above the clivus, some ligament bundles joined the contralateral petrosphenoidal ligament, whilst another group of bundles originated at the posterior clinoid process. At the entry to Dorello’s canal, the abducens nerve had a diameter of 0.59 mm on the left and 0.65 mm on the right. The part of the ligaments converging on the clivus in the midline after dividing into two arms was 10.68 mm. We think that this case report will provide useful information for surgical procedures to the petroclival region, transnasal surgical approaches, and surgical interventions involving the carotid artery.


Introduction
The petrosphenoidal ligament is also known as the Gruber ligament or the posterior petroclinoid ligament. This ligament was initially defined by Wenzel Gruber in 1859 [16]. It can be Y-shaped, duplicated, or formed like a triangle or butterfly in a single band and usually extends anteriorly from the posterior clinoid process (PCP) or upper lateral part of the clivus to the petrous apex [2,3,8,12] (Fig. 1). The narrow ends of the center of the petrosphenoidal ligament were butterfly-shaped in 78% of the samples investigated by Icke et al. [2]. This ligament forms the superolateral border of Dorello's canal, first defined by Primo Dorello in 1905 [8,16]. It has served as a significant marker in surgical procedures. The contents of Dorello's canal include the inferior petrosal sinus, abducens nerve, and the dorsal meningeal branch of the meningohypophyseal trunk in most individuals [8]. In addition, at the petrous apex and petroclival region, the petrosphenoidal ligament is closely associated with the anterior clinoid process, internal carotid artery, basilar plexus, dorsum sellae, meningohypophyseal trunk, oculomotor nerve, trochlear nerve, trigeminal ganglion, and branches of the trigeminal nerve [2,3,8].
The abducens nerve has three parts that run from the brainstem to the orbit. The first is located in the subarachnoid space, where the nerve proceeds from the bulbopontine sulcus to the dura mater, laterally to the clivus. The second part is situated on the lateral to the internal carotid artery, within the cavernous sinus inside the cavernous sinus. The third part enters the orbit via the superior orbital fissure, and finally reaches the lateral rectus muscle [5,9]. The abducens nerve passes to the second part through Dorello's canal, which is situated beneath the petrosphenoidal ligament. The abducens nerve follows a lengthy intracranial course. The transverse branches of the basilar artery or the sharp upper borderline of the petrous apex may compress the abducens nerve, which is very sensitive to such traumas [9,16]. Additionally, the petrosphenoidal ligament may ossify completely or partially, resulting in abducens nerve palsy [1,6]. The petrosphenoidal ligament is important in skull base surgery due to its close proximity to several anatomical structures, such as the dorsal meningeal artery and abducens nerve. It is highly important for the microanatomy of the petroclival region to be known exactly in surgical procedures to be performed on the clivus, cavernous sinus, and petroclival region [2,3]. This report described the attachment of the petrosphenoidal ligament, which originates from the PCP and joins with the contralateral ligament on the clivus, in newborn cadavers, a subject which, to the best of our knowledge, has not been presented before. We think that our report may be of particular cognitive and practical value since the petrosphenoidal ligament is an important anatomical landmark during neurosurgical procedures.

Case report
The anatomy of the petrosphenoidal ligament was studied in 10 formalin-fixed newborn cadavers at the Ondokuz Mayıs University Faculty of Medicine Department of Anatomy, Turkey.
Twenty ligaments, 10 right-and 10 left-side, obtained from the cadavers were used in the study. The petrosphenoidal ligament and abducens nerve were examined. Dissections were performed in the Department of Anatomy dissection laboratories. This study was carried out with the approval of the Ondokuz Mayıs University Clinical Research Ethics Committee (Decision no. 2022/390). The following procedures were performed on each newborn cadaver.
To open the skull base, a horizontal peripheral skin incision was first made around the head from 10 mm above the upper border of the orbit, extending from the glabella in the front to the inion in the back. The skin was then removed to expose the calvaria. Craniotomy was then performed using bone scissors, after which calvaria was removed, and the dura mater appeared. The dura mater was opened, and both cerebral hemispheres were removed. The tentorium cerebelli was then dissected, and the cerebellum was removed at the medulla oblongata level [3]. The petrosphenoidal ligament and abducens nerve were dissected and visualized. Dissection procedures were performed with the aid of a LEICA CLS 100 stereo microscope.
An atypical termination of the right and left petrosphenoidal ligaments was observed during routine dissection of one of the newborn cadavers. The right and left petrosphenoidal ligaments were connected at the midline of the clivus (Fig. 1). The ligaments were Y-shaped, and the attachment of the proximal ligaments was bifid (Figs. 2 and 3). In the midline above the clivus, some ligament bundles joined the contralateral petrosphenoidal ligament, whilst another group of bundles originated at the PCP. The abducens nerve passed through the lateral third of Dorello's canal under the petrosphenoidal ligament on the left side. On the right side, it passed under the petrosphenoidal ligament in the middle third of Dorello's canal (Fig. 2). The dorsal meningeal artery passed under the petrosphenoidal ligament medial to the abducens nerve (Fig. 3). The length of the right and left ligaments to the point where it splits into two arms, the joint length of the two ligaments at the junction of the clivus, the length of the ligament leading to the PCP, and the abducens nerve's diameter as it passes below the ligament were measured on ImageJ software.
The diameter of abducens nerve at the entrance to Dorello's canal was 0.65 mm on the right and 0.59 mm on the left. The part of the ligaments converging on the clivus in the midline after dividing into two arms was 10.68 mm in length. On the right and left, the ligaments arm that extends the PCP measured 2.69 mm and 2.78 mm, respectively. The length of the ligament starting from the petrous apex to the part where it splits into two branches was 2.81 mm on the left and 2.90 mm on the right.

Discussion
Before the surgical interventions to be applied to the clivus, petroclival region and cavernous sinus, it is necessary to have detailed information about the microanatomy of these regions. The developmental process of the clivus causes some differences between adult and newborn cadavers. At birth, the clivus consists of two parts, the basioccipital and basisphenoid, which are partially ossified. These two parts are separated from each other by spheno-occipital synchondrosis. This structure is the main region that provides the longitudinal growth of the skull base [13]. Complete ossification of synchondrosis and termination of longitudinal growth of the skull base occurs at 13-18 years of age in males and 12-16 years in females [7,13]. The petrosphenoidal ligament is a structure formed during the development of the dura mater in the embryological period. This ligament is the fold of the dura mater and is located between the meningeal and periosteal layers of the dura mater. Consisting of collagen and elastic fibers, this ligament is densely packed into fascicles. The abducens nerve sheath is fixed in the petroclival region by the petrosphenoidal ligament. It is an important landmark during anterior petrosectomy. It takes on the task of protecting the abducens nerve and prevents damage to the wound. [8,10,14]. Although the petrosphenoidal ligament is an important anatomical landmark, its microanatomical features are still not fully elucidated [3,8].
Previous studies have revealed that the ligament may exhibit a number of variations. The ligament has been described as being in the form of a butterfly or triangularshaped single band and attached to the bone or anterior part of the dura mater in 58.1% of cases. In 32.3% of the cases, the ligament was Y-shaped and attached anteriorly to both the clivus and the dura mater. The ligament was  reported as duplicated in 9.7% of cases [3]. In a recent study, 36 sides of eighteen fresh-frozen adult cadaver heads were examined to find out which variations occur and what morphologic characteristics the petrosphenoidal ligament has. They found that the petrosphenoidal ligament's anterior attachment is primarily to the upper extension of the clivus (rather than the PCP). Therefore, the authors suggested renaming the petrosphenoidal ligament as the petroclival ligament [1,3]. Another recent study examined 297 ligaments in total to identify the location of the petrosphenoidal ligament's anterior attachment to the bone. The most typical anterior attachment point was found to have a prevalence of 72.95% at the PCP [12]. Therefore, we used the term petrosphenoidal ligament in this study. In the present case, the petrosphenoidal ligament was Y-shaped and attached to the PCP and clivus. However, the branch of the ligament above the clivus merged with the branch of the contralateral ligament.  [3,9]. In our cadaver, the abducens nerve's diameter was 0.65 mm on the right and 0.59 mm on the left.
Ozer et al. found that abducens nerve passed under the middle third of the petrosphenoidal ligament in five cases (12.5%) and under the lateral third in 33 (82.5%) [9]. Iwanaga et al. reported that the abducens nerve passed under the middle third of the petrosphenoidal ligament in 12 cases (38.7%) and under the lateral third in 19 (61.3%) [3]. Joo et al. found that the abducens nerve passed under the lateral third of the ligament in 95% of their 20 cadavers [5]. In all three studies, the abducens nerve did not pass under the medial third of the ligament in any sample [3,5,9]. Kayacı et al. reported that the abducens nerve was located under the medial side of the ligament in the pediatric group and under the lateral edge in the adult group [6]. In our cadaver, the left abducens nerve passed under the lateral third of the ligament, while the right abducens nerve passed under the middle third. Ozer et al. reported that the abducens nerve was duplicated before passing under the petrosphenoidal ligament and entered Dorello's canal in 10% of the 20 cases they examined [9]. In their study of 50 specimens, Ozveren et al. reported that the abducens nerve was duplicated before reaching the petrosphenoidal ligament in two specimens, with one branch passing under the petrosphenoidal ligament and the other over it [11]. Several case reports involving the petrosphenoidal ligament have been presented previously. Gutierrez et al. revealed that the left petrosphenoidal ligament was ossified in adult male cadavers. They also found that there was a foramen in the bone where the abducens nerve entered the cavernous sinus below the petrosphenoidal ligament [1]. Tubbs et al. identified bilateral ossification of the petrosphenoidal ligament and emphasized that clinicians should take the petrosphenoidal ligament ossification into consideration in abducens nerve palsy of unknown cause [15]. Zytkowski et al. described the dual origin of the Y-shaped petrosphenoidal ligament to the clivus and posterior genus of the internal carotid artery in their case report [17]. Those authors stated that this relationship between the ligament and the carotid artery would cause atypical fixation of both structures. They described this is as particularly important as it could potentially change some surgical procedures, such as mobilization of the short vertical segment of the internal carotid artery and its posterior genus [15,17].
As shown in these studies and the present report, the morphology of the petrosphenoidal ligament and its relationship with the abducens nerve and other structures may rarely differ. The petrosphenoidal ligament is an important marker for the abducens nerve in transnasal surgical approaches and for surgical procedures to the carotid artery [15,17]. Prior knowledge of the possible variations of the petrosphenoidal ligament and adjacent anatomical structures will thus increase the success of the surgical procedure.

Conclusions
To the best of our knowledge, the present report represents the first case in which the petrosphenoidal ligament in a newborn cadaver was both Y-shaped and joined with the contralateral ligament. The petroclival region, in which the petrosphenoidal ligament is located, is dense in vessels and nerves. The site of the ligament here is very important in determining the locations of the sinus cavernosus, internal carotid artery, and cranial nerves. We think that using the petrosphenoidal ligament as a reference point in surgical procedures in this area and knowing the possible variations that can be seen in it will be very useful for surgeons in clinical practice. and their families deserve our highest gratitude [4]. Also, we would like to thank The Scientific and Technological Research Council of Turkey for their support within the scope of the 2211-A General Doctorate Scholarship.
Author contributions BOK: project development, data collection and management, data analysis and manuscript writing. AAW: project development, data collection, manuscript writing and manuscript editing. OB: project development, methodology, data analysis and manuscript writing. ME: manuscript editing. SB: manuscript editing. All the authors have read and approved the manuscript.

Funding
The authors did not receive support from any organization for the submitted work.

Data availability
The data used to support the findings of this study are available from the corresponding author upon reasonable request.