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Child's Nervous System

, Volume 34, Issue 8, pp 1451–1458 | Cite as

A comprehensive review of the clivus: anatomy, embryology, variants, pathology, and surgical approaches

  • Rabjot Rai
  • Joe Iwanaga
  • Ghaffar Shokouhi
  • Marios Loukas
  • Martin M. Mortazavi
  • Rod J. Oskouian
  • R. Shane Tubbs
Review Paper

Abstract

Introduction

The clivus is a bony structure formed by the fusion of the basioccipital and basispheniod bone at the sphenooccipital synchondrosis. This downward sloping structure from the dorsum sellae to the foramen magnum is derived from mesoderm and ectoderm properties.

Methods

This comprehensive review of the clivus will discuss its basic anatomy, embryology, pathological findings, and surgical implications. The clivus is an endochondral bone, formed under two processes; first, a cartilaginous base is developed, and it is secondly reabsorbed and replaced with bone. Knowledge of its embryological structure and growth of development will clarify the pathogenesis of anatomical variants and pathological findings of the clivus.

Conclusions

Understanding the anatomy including proximity to anatomical structures, adjacent neurovasculature properties, and anatomical variants will aid neurosurgeons in their surgical management when treating pathological findings around the clivus.

Keywords

Clivus Skull base Notochord Anatomy Embryology Surgery 

Introduction

The clivus (Latin: slope or hill) (Figs. 1 and 2) is an important structure situated at the central base of the skull. The clivus (also known as Blumenbach’s clivus after German physiologist and anthropologist Johann Friedrich 1752–1840) is a bony structure formed when the basal portion of the occipital bone, the basioccipital, combines with the body of the sphenoid bone, the basisphenoid, at the sphenooccipital synchondrosis [10]. This bone slants upward and forward from the anterior aspect of foramen magnum to the posterior clinoid processes [3, 7, 10]. Understanding the anatomical variants and pathologies associated with the clivus requires extensive knowledge regarding the basic anatomy and embryology of the clivus.
Fig. 1

Inferior view of fetal skull base noting the clivus and its sphenoid (S) and occipital (O) parts. Note the intervening spheno-occipital synchondrosis (SOS). For reference, also note the occipital condyles (OC) and foramen magnum (FM)

Fig. 2

Left: midsagittal section through a cadaveric specimen noting the clivus (yellow line). Note the relationships with it and surrounding structures such as the pons and medulla oblongata. Right: hemisected skull noting the clivus (black line) and its relationship with the upper cervical spine

Anatomy

The clivus is a central configuration of the skull base and measures about 4 to 5.5 cm long and about 3 cm wide at its midpoint. Its angulation is varied but is on average, 116°. When addressing the anatomy of the clivus, it is vital to understand its location in terms of adjacent structures. The clivus descends inferiorly from the dorsum sellae to the anterior border of the foramen magnum (Fig. 3) [13]. The anterior border of the clivus, on the other hand, is not as distinct as it blends with the sphenoid bone adjacent the sphenoidal sinus [10]. Lateral to the clivus is the petro-occipital fissure housing the inferior petro-occipital vein connecting the cavernous sinus to the internal jugular vein (Fig. 3) [10, 13]. The lateral borders of the clivus are related to cranial nerves V through XII, the internal jugular veins, and the inferior petrosal sinuses (Fig. 4) [3]. The basal subarachnoid space anterior to the brain stem is related to its posterior surface [13]. The medulla oblongata and pons lie adjacent to the posterior surface of the clivus, but are separated by the prepontine and perimedullary cisterns (Fig. 2). The tectorial membrane and superior longitudinal band of the cruciate ligament both attach to the posteroinferior surface of the clivus (Fig. 5). The tectorial membrane is an extension of the posterior longitudinal ligament, which extends from the posterior surface of the bodies of C1-C2 toward the clivus [10].
Fig. 3

Internal view of left hemisected skull noting the clivus and some related anatomical structures such as the sigmoid sinus (SS), internal auditory meatus (IAM), dorsum sellae (SD), and petro-occipital fissure (POF)

Fig. 4

Schematic drawings of the clivus and surrounding neurvasculature. Left: note the optic chiasm (OC) and trigeminal ganglion (V) and wedged between them, the oculomotor and trochlear nerves. At the clivus, not the abducens nerve (VI) entering Dorello’s canal and in blue, the basilar venous plexus. Right: note the exposed course of the right abducens nerve (VI) on the clivus (the overlying clival dura is removed on the right side of this image) compared to its extra and intradural parts on the left side. The basilar venous plexus is seen as is the trigeminal (V) and oculomotor (III) nerves

Fig. 5

Midsagittal view of the craniocervical junction noting the ligamentous attachments onto the clivus and specifically, its basioccipital part (B). From the apex of the odontoid process (OP) note the apical ligament (AL). The anterior atlanto-occipital membrane (AAOM) is seen as a continuation of the anterior longitudinal ligament up to the clivus. Note the superior band (SB) of the cruciate ligament extending superiorly to the basion and covered posteriorly by the tecotoiral membrane (pink)

The clivus takes on a concave shape when viewed posterosuperiorly and is more prominent inferiorly at the location of the jugular tubercles, which project on the lateral inferior margins of the clivus [3, 10]. The fibrous raphe of the pharynx (superior pharyngeal constrictor muscle), longus capitus, rectus capitus anterior, and the anterior atlanto-occipital membrane are found in connection to the inferior surface, exocranial part, of the clivus [10]. The posterior surface, endocranial part, of the clivus is smooth, composed of cortical bone, and is covered with dura mater [7, 10]. On a midsagittal section, the clivus is a wedged shaped bone, which is thicker anteriorly and becomes thinner posteriorly [7]. Close examination of the central portion of the clivus demonstrates cancellous bone containing bone marrow, which may be variably pneumatized [7, 10, 13].

Embryology

Understanding the embryology of the clivus may explain pathologies that occur in the region secondary to developmental remnants. The mesoderm and ectoderm are both involved in the development of the skull base; mesoderm develops into the posterior cranial fossa base, and neural crest cells are involved in the growth of parts anterior to the notochord [4]. The skull base is composed of vertebral parts; this includes the notochord (chorda dorsalis), which ends at the junction below the dorsum sellae [7]. The clivus is an endochondral bone; its progression involves cartilaginous formation followed by reabsorption preceding bone deposition [17].

During development, the notochord follows an intricate path where it exits the skull base to the outer surface of the future clivus and where irregular processes are produced (Fig. 6) [7]. At the basisphenoid, the notochord enters and reaches the caudal extent of the hypophysis where the cranial base begins its development [12]. A thick mass of mesenchyme surrounds the brain, appearing first in the occipital side, and enclosing the notochord as it moves toward the hypophysis to contour the clivus and dorsum sellae; this is known as the membranous stage. Due to the abundance of sulfated glycosaminoglycan at the rostral tip of the notochord, it initiates the process of condensation and chondrification of the occipital sclerotome-derived mesenchyme forming the parachordal cartilage; this is known as the cartilaginous stage. The initial chondrification centers commence at the basioccipital and extend toward the cartilaginous centers of the future basal extent of the sphenoid bone [13]. By the sixth week of development, the basisphenoid includes two ossification centers, and by the seventh week, the basioccipital portion of the occipital bone is developed [4, 13]. At birth, the clivus is composed of partially ossified basioccipital and basisphenoid parts separated by the spheno-occipital synchondrosis [12].
Fig. 6

Upper: embryological components contributing to the craniocervical junction. Note the hypochordal bow of sclerotome 4 (S4) forming the basiocciput of the clivus. Lower: note the pathway of the notochord through the axis and up into and around the clivus

The clivus remains a heterogeneous structure divided by the spheno-occipital synchondrosis until adolescence [10]. This structure remains a staple as a growth zone, as it is a primary region for the longitudinal growth of the skull base. Complete ossification of the synchondrosis (Fig. 7) takes place at the age of 13 to 18 years in males and 12 to 16 years in females [15].
Fig. 7

Axial (left) and sagittal (right) CT images of the skull base. Note the spheno-occipital synchondrosis (arrows). The contribution of the basiocciput part (BO) of the clivus and its contribution to the skull base, and in particular, the anterior aspect of the foramen magnum is seen at left

The anterior arch of the atlas is an embryological structure relating to the hypochordal blastemas. It is a part of the skull base, and during the development of the hypochordal blastemas, the proatlas and other vertebral levels are subsequently absorbed (Figs. 6 and 8). However, failure of reabsorption can lead to variation at the caudal end of the clivus [7].
Fig. 8

Developmental derivations of the craniocervical junction noting the lower clivus origin from the 4th occipital sclerotome (dark blue)

Anatomical variants

As mentioned earlier, the clivus is developed from the fusion of the basiocciput and basisphenoid across the spheno-occipital synchondrosis. This portion of the central skull base has variations to its structure based on its development. A study conducted by DiChiro and Anderson (1965) observed 94 cadaver skulls in normal adults and found the majority (77.66%) had a slight concavity of the clivus surface of mostly 1 to 2 mm with a few outliers of 3 mm. From the remainder of the population, 19% had a flat clivus, and 0.03% had a convex clivus. The study also noted occasionally findings of more than 4-mm concavity in the posterior portion of the clivus in patients with posterior fossa tumors and conditions causing longstanding increased intracranial pressure. Other changes noted in the clivus include grooves from the overlying basilar artery with an incidence of 1% [13, 16].

Basilar impression is softening of surrounding bones such as the clivus and is due to, for example, osteoporosis, rickets, and von Recklinghausen disease [16]. Clival scalloping is sometimes seen in the Chiari II malformation [22]. Platybasia is another variation where the clivus is positioned more horizontally, causing the sphenoidal angle to widen. This angle enlargement can be due to elevation of the dorsal or frontal side of the angle [16].

A shortened clivus is a typical finding in all patients with achondroplasia and Chiari II malformation. In patients with idiopathic, or without achondroplasia, findings of a shortened clivus can be attributed toward the premature merging or due to reduced developmental growth of the spheno-occipital synchondrosis [13].

Rare anatomical variants of the clivus include Sauser’s fissure, also known as the basilar transverse fissure. Its development may be present on one or both sides and can be formed either completely or partially. The basilar fissure may distinguish the margin of the basioticum and basioccipital bones contingent upon the development of the basilar portion of the occipital bone [7, 23].

The basilar processes are variants seen in 4% of the population; they consist of unilateral or bilateral small bony protuberance at the anterior boundary of the foramen magnum. It is believed that their pathogenesis is derived from remnants of the lateral hypochordal blastema of the proatlas. In rare occurrences, the larger basilar processes communicate with the anterior arch of the atlas resulting in instability of the atlantooccipital joint [7]. If the hypochordal blastema of the proatlas persisted in the medial aspect, it would give rise to a third condyle at the anterior margin of the foramen magnum [16]. A much scarcer variant is the arcus praebasioccipitalis occurring in 0.03% of the population. It is an osseous mass in the shape of a horseshoe positioned at the anterior margin of the foramen magnum formed by the complete persistence of the hypochordal blastemas. It may affect the functioning of the craniovertebral joints.

The presences of bony canals through the clivus (Fig. 9) are suggested to contain communicating vessels with the internal and external venous plexus. When the basal segment of the occipital canal contains a bony canal known as basilar canalis, it may carry a previous basivertebral veins originating from the vertebral material integrated into the skull base. It is present among 8% of the population; however, the median basilar canalis, which emerges from the midline of the basiocciput, has a prevalence of 20% in newborns and is rarely seen in adults, only 1%. The embryology of the basilar canals is suggested to be (1) vascular origins or (2) remnants of the notochord [8]. However, Sheikh et al. presented a case report of a fossa navicularis, a subtype of the basilar canalis, and found no indication of lymphoidal, glandular, or notochord tissue upon histological analysis. In this case, the composition of the fossa navicularis was loose connective tissue, collagen, and elastic fibers, with vascular origins of veins, arteries, and capillaries [21].
Fig. 9

Skeletal sample of the basiocciput noting clival canals. One canal seen at left is filled with a pipe cleaner for clarity. Another canal on the right is seen at the arrow

The apical ligament (Fig. 5) ascends from the apex of the dens to anterior margin (basion) of the foramen magnum. If ossified, it can present as a bony spur on the clivus [6, 7]. Another adaptation includes the ossification of the enclosed material while the core remains ligamentous, resulting in a tube-like development instead of spur [7].

Arterial supply and venous relationships

The arterial supply of the clivus (Fig. 10) is primarily derived from two vessels. The first is a branch off the internal carotid artery, the meningohypophyseal trunk, and the second main vessel is a branch of the ascending pharyngeal artery, the posterior meningeal artery [18]. There are many variations regarding the meningohypophyseal trunk in terms of its branching and anastomoses [25]. The meningohypophyseal trunk gives off the dorsal meningeal artery, which passes posteriorly through the cavernous sinus, within Dorello’s canal with the abducens nerve and the inferior petrosal sinus, to supply the clival dura mater. Alongside the inferior petrosal sinus runs the lateral clival artery, which anastomosis with the posterior meningeal artery. The medial group of branches supplies the apex of the clivus to the height of where the abducens nerve emerges. A branch of the ascending pharyngeal artery, the posterior meningeal artery, passes through the jugular foramen and enters the posterior cranial fossa supplying the inferior dura mater of the clivus [18]. The blood supply of the clivus is clinically significant due to the implications of tumors. Dorsal to the clivus, the basilar artery and basilar venous plexus are found and can create faint grooves on the bone [3]. Since the original development of the basilar venous plexus (Fig. 4) is related to the vertebral column, it is considered a constituent of Batson’s plexus [7].
Fig. 10

Blood supply to the clivus derived from the meninohypophyseal trunk, which is shown here providing clival and meningeal (dorsal meningeal) branches

Pathology

Non-neoplastic tumors

Fibrous dysplasia

Fibrous dysplasia is a benign skeletal anomaly that may affect one or multiple bones, with a greater tendency to affect long bones, ribs, and craniofacial bones [2]. The mature bone becomes replaced with a weaker substitute of woven bone and fibrous tissue. More commonly, the disorder affects a single bone in 70% of cases and multiple bones in 30% [1]. McCune-Albright syndrome involves multiple bone subtype of fibrous dysplasia, café-au-lait spots, and endocrine disorders, in which the clivus and sphenoid bone may be involved [14]. Imaging with a ground glass appearance is pathognomonic for fibrous dysplasia.

Neurenteric cyst

If CT images display an integral cortex with lytic lesions, it should raise concerns of a possible neurenteric cyst [7]. A location at the clivus is unusual but not surprising given that the embryological nature involves dysgenesis of the notochord during early development [11].

Ecchordosis physaliphora

Ecchordosis physaliphora is a congenital hamartomatous lesion derived from notochord remnants and is seen in approximately 2% of the population. It is located in the retroclival region and projects toward the intradural prepontine cistern. The tissue appears hypotense on T1-weighted MRI and hypertense on T2-weighted MRI with a lack of contrast enhancement compared to other tumors such as chordomas. The clinical repercussion of this tumor-like mass is bleeding or CSF leakage [7].

Neoplastic tumors

Meningioma

The dorsal dural surface of the clivus increases its propensity of being affected by meningiomas. Due to the lack of arachnoid granulations at the central aspect of the clivus, meningiomas arise more commonly at the petroclival line. As a result, meningiomas are often located medial to the trigeminal nerve [7, 20]. When excising the tumor, neurosurgeons must be attentive toward the vasculature surrounding the mass.

Chordomas

Chordomas are similar to ecchordosis physaliphora in that they are both relics of notochordal tissue. The direction of travel of the notochord from the odontoid process moving anteriorly toward the basiocciput can lead to susceptibility of notochord remnants within the area and lead to the development of chordomas [24]. However, compared to ecchordosis physaliphora, chordomas are malignant tumors arising within the bone in a slow growing manner with a potential to metastasize via lymphatics or hematogenously [7]. Chordomas are uncommon and account for less than 1% of all intracranial tumors [24]. They have a greater prevalence in males by the third and fourth decades of life and commonly occur is the sacrum, clivus, and cervical vertebrae. Approximately one-third occur at the clivus originating within the bone as a well circumcised, midline extradural soft-tissue mass and often affecting the abducens nerve at initial presentation [5]. On imaging, clival chondromas appear as soft tissue masses with lytic bone destruction. Due to high fluid content of the chordomas, on T1-weighted MRI, they appear hyperintense, while on T2-weighted MRI, they appear hypotense (as opposed to ecchordosis physaliphora) with moderate degree of contrast enhancement [7]. Treating chordomas are difficult as they often recur and occupy a difficult location in terms of neighboring neurovascular structures. Clival chordomas sit in close proximity to the brain stem, thus compressive growth and inadequately managed tumors often lead to high morbidity and mortality [26].

Surgical approaches

The location of masses on the clivus presents a challenge to surgeons who must maintain vital structures adjacent to it including the pituitary gland, internal carotid artery, cavernous sinus, basilar artery, and brain stem. With slow growing tumors such as chordomas, the extension of the tumor to surrounding structures is already compromised during initiation of symptoms and creates another barrier for surgeons to achieve clear margins.

When accessing a clival mass, craniotomies usually require excessive brain retraction, which can lead to complications including cerebral infarction, hematoma, and regional brain atrophy. Additionally, these approaches do not give access to extradural portions of the tumor. The microscopic transsphenoidal approach allows for better visualization of the sella turcica and upper to middle clivus [18]. The lower clivus and craniocervical junction (CCV) are not adequately viewed, as they would be with a transoral approach. This approach is limited, preventing access to the upper clivus, pharyngeal space, and jugular foramen. However, a maxillary osteotomy allows for access to the upper, middle, and lower clival regions and the CCV. However, the maxillary osteotomy approach requires a facial incision, which may cause dysfunction and deformities to adjacent regions. Lastly, the endoscopic approach to the clivus provides a complete 360-degree view of the clivus and its adjacent structures allowing for complete resection of the tumor. This approach is not without its limitations as it is more likely to cause intracranial infection. The endoscopic technique provides an off-center line of sight of the clivus, although this can be conquered by the surgeon’s knowledge of clival anatomy and practical skills using the endoscope [9].

Conclusion

The clivus is adjacent to important anatomical structures, which makes surgical approaches to this region complicated. The embryology of the clivus highlights the intricate course of the notochord, and how remnants of the notochord may lead to the development of pathological findings. Understanding the anatomy and adjacent neurovasculature structures and anatomical variants will aid skull base surgeons in their management when treating pathological findings around the clivus.

Notes

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Rabjot Rai
    • 1
  • Joe Iwanaga
    • 2
  • Ghaffar Shokouhi
    • 3
  • Marios Loukas
    • 1
  • Martin M. Mortazavi
    • 4
  • Rod J. Oskouian
    • 5
  • R. Shane Tubbs
    • 1
    • 2
  1. 1.Department of Anatomical SciencesSt. George’s UniversitySt. George’sGrenada
  2. 2.Seattle Science FoundationSeattleUSA
  3. 3.Neurosciences Research CenterTabriz University of Medical SciencesTabrizIran
  4. 4.California Institute of NeuroscienceThousand OakesUSA
  5. 5.Swedish Neuroscience InstituteSeattleUSA

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