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Child's Nervous System

https://doi.org/10.1007/s00381-018-3875-x

REVIEW PAPER

A comprehensive review of the clivus: anatomy, embryology, variants,


pathology, and surgical approaches
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

Received: 14 June 2018 / Accepted: 18 June 2018


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

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 variants and pathologies associated with the clivus requires


extensive knowledge regarding the basic anatomy and embry-
The clivus (Latin: slope or hill) (Figs. 1 and 2) is an important ology of the clivus.
structure situated at the central base of the skull. The clivus
(also known as Blumenbach’s clivus after German physiolo-
gist and anthropologist Johann Friedrich 1752–1840) is a Anatomy
bony structure formed when the basal portion of the occipital
bone, the basioccipital, combines with the body of the sphe- The clivus is a central configuration of the skull base and
noid bone, the basisphenoid, at the sphenooccipital measures about 4 to 5.5 cm long and about 3 cm wide at its
synchondrosis [10]. This bone slants upward and forward midpoint. Its angulation is varied but is on average, 116°.
from the anterior aspect of foramen magnum to the posterior When addressing the anatomy of the clivus, it is vital to un-
clinoid processes [3, 7, 10]. Understanding the anatomical derstand its location in terms of adjacent structures. The clivus
descends inferiorly from the dorsum sellae to the anterior bor-
der of the foramen magnum (Fig. 3) [13]. The anterior border
* Joe Iwanaga of the clivus, on the other hand, is not as distinct as it blends
joei@seattlesciencefoundation.org
with the sphenoid bone adjacent the sphenoidal sinus [10].
Lateral to the clivus is the petro-occipital fissure housing the
1
Department of Anatomical Sciences, St. George’s University, St. inferior petro-occipital vein connecting the cavernous sinus to
George’s, Grenada
the internal jugular vein (Fig. 3) [10, 13]. The lateral borders
2
Seattle Science Foundation, 550 17th Ave, James Tower, Suite 600, of the clivus are related to cranial nerves V through XII, the
Seattle, WA 98122, USA
internal jugular veins, and the inferior petrosal sinuses (Fig. 4)
3
Neurosciences Research Center, Tabriz University of Medical [3]. The basal subarachnoid space anterior to the brain stem is
Sciences, Tabriz, Iran
related to its posterior surface [13]. The medulla oblongata
4
California Institute of Neuroscience, Thousand Oakes, CA, USA and pons lie adjacent to the posterior surface of the clivus,
5
Swedish Neuroscience Institute, Seattle, WA, USA but are separated by the prepontine and perimedullary cisterns
Childs Nerv Syst

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. 1 Inferior view of fetal skull base noting the clivus and its sphenoid cortical bone, and is covered with dura mater [7, 10]. On a
(S) and occipital (O) parts. Note the intervening spheno-occipital midsagittal section, the clivus is a wedged shaped bone, which
synchondrosis (SOS). For reference, also note the occipital condyles
(OC) and foramen magnum (FM)
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 var-
(Fig. 2). The tectorial membrane and superior longitudinal iably pneumatized [7, 10, 13].
band of the cruciate ligament both attach to the posteroinferior
surface of the clivus (Fig. 5). The tectorial membrane is an Embryology
extension of the posterior longitudinal ligament, which ex-
tends from the posterior surface of the bodies of C1-C2 toward Understanding the embryology of the clivus may explain pa-
the clivus [10]. thologies that occur in the region secondary to developmental
The clivus takes on a concave shape when viewed remnants. The mesoderm and ectoderm are both involved in
posterosuperiorly and is more prominent inferiorly at the lo- the development of the skull base; mesoderm develops into
cation of the jugular tubercles, which project on the lateral the posterior cranial fossa base, and neural crest cells are in-
inferior margins of the clivus [3, 10]. The fibrous raphe of volved in the growth of parts anterior to the notochord [4]. The
the pharynx (superior pharyngeal constrictor muscle), longus skull base is composed of vertebral parts; this includes the
capitus, rectus capitus anterior, and the anterior atlanto- notochord (chorda dorsalis), which ends at the junction below
occipital membrane are found in connection to the inferior the dorsum sellae [7]. The clivus is an endochondral bone; its
surface, exocranial part, of the clivus [10]. The posterior sur- progression involves cartilaginous formation followed by re-
face, endocranial part, of the clivus is smooth, composed of absorption preceding bone deposition [17].

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
Childs Nerv Syst

Fig. 4 Schematic drawings of the clivus and surrounding right abducens nerve (VI) on the clivus (the overlying clival dura is
neurvasculature. Left: note the optic chiasm (OC) and trigeminal ganglion removed on the right side of this image) compared to its extra and
(V) and wedged between them, the oculomotor and trochlear nerves. At intradural parts on the left side. The basilar venous plexus is seen as is
the clivus, not the abducens nerve (VI) entering Dorello’s canal and in the trigeminal (V) and oculomotor (III) nerves
blue, the basilar venous plexus. Right: note the exposed course of the

During development, the notochord follows an intricate basioccipital and extend toward the cartilaginous centers of
path where it exits the skull base to the outer surface of the the future basal extent of the sphenoid bone [13]. By the sixth
future clivus and where irregular processes are produced week of development, the basisphenoid includes two ossifica-
(Fig. 6) [7]. At the basisphenoid, the notochord enters and tion centers, and by the seventh week, the basioccipital portion
reaches the caudal extent of the hypophysis where the cranial of the occipital bone is developed [4, 13]. At birth, the clivus is
base begins its development [12]. A thick mass of mesen- composed of partially ossified basioccipital and basisphenoid
chyme surrounds the brain, appearing first in the occipital parts separated by the spheno-occipital synchondrosis [12].
side, and enclosing the notochord as it moves toward the hy- The clivus remains a heterogeneous structure divided by
pophysis to contour the clivus and dorsum sellae; this is the spheno-occipital synchondrosis until adolescence [10].
known as the membranous stage. Due to the abundance of This structure remains a staple as a growth zone, as it is a
sulfated glycosaminoglycan at the rostral tip of the notochord, primary region for the longitudinal growth of the skull base.
it initiates the process of condensation and chondrification of Complete ossification of the synchondrosis (Fig. 7) takes
the occipital sclerotome-derived mesenchyme forming the place at the age of 13 to 18 years in males and 12 to 16 years
parachordal cartilage; this is known as the cartilaginous stage. in females [15].
The initial chondrification centers commence at the 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 blaste-
mas, the proatlas and other vertebral levels are subsequently

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 Fig. 6 Upper: embryological components contributing to the
up to the clivus. Note the superior band (SB) of the cruciate ligament craniocervical junction. Note the hypochordal bow of sclerotome 4 (S4)
extending superiorly to the basion and covered posteriorly by the forming the basiocciput of the clivus. Lower: note the pathway of the
tecotoiral membrane (pink) notochord through the axis and up into and around the clivus
Childs Nerv Syst

Fig. 7 Axial (left) and sagittal


(right) CT images of the skull ba-
se. Note the spheno-occipital
synchondrosis (arrows). The con-
tribution of the basiocciput part
(BO) of the clivus and its contri-
bution to the skull base, and in
particular, the anterior aspect of
the foramen magnum is seen at
left

absorbed (Figs. 6 and 8). However, failure of reabsorption can occipital synchondrosis. This portion of the central skull base
lead to variation at the caudal end of the clivus [7]. has variations to its structure based on its development. A
study conducted by DiChiro and Anderson (1965) observed
Anatomical variants 94 cadaver skulls in normal adults and found the majority
(77.66%) had a slight concavity of the clivus surface of mostly
As mentioned earlier, the clivus is developed from the fusion 1 to 2 mm with a few outliers of 3 mm. From the remainder of
of the basiocciput and basisphenoid across the spheno- the population, 19% had a flat clivus, and 0.03% had a convex

Fig. 8 Developmental
derivations of the craniocervical
junction noting the lower clivus
origin from the 4th occipital
sclerotome (dark blue)
Childs Nerv Syst

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 Fig. 9 Skeletal sample of the basiocciput noting clival canals. One canal
or frontal side of the angle [16]. seen at left is filled with a pipe cleaner for clarity. Another canal on the
A shortened clivus is a typical finding in all patients with right is seen at the arrow
achondroplasia and Chiari II malformation. In patients with
idiopathic, or without achondroplasia, findings of a shortened suggested to be (1) vascular origins or (2) remnants of the
clivus can be attributed toward the premature merging or due notochord [8]. However, Sheikh et al. presented a case report
to reduced developmental growth of the spheno-occipital of a fossa navicularis, a subtype of the basilar canalis, and
synchondrosis [13]. found no indication of lymphoidal, glandular, or notochord
Rare anatomical variants of the clivus include Sauser’s fis- tissue upon histological analysis. In this case, the composition
sure, also known as the basilar transverse fissure. Its develop- of the fossa navicularis was loose connective tissue, collagen,
ment may be present on one or both sides and can be formed and elastic fibers, with vascular origins of veins, arteries, and
either completely or partially. The basilar fissure may distin- capillaries [21].
guish the margin of the basioticum and basioccipital bones The apical ligament (Fig. 5) ascends from the apex of the
contingent upon the development of the basilar portion of dens to anterior margin (basion) of the foramen magnum. If
the occipital bone [7, 23]. ossified, it can present as a bony spur on the clivus [6, 7].
The basilar processes are variants seen in 4% of the popu- Another adaptation includes the ossification of the enclosed
lation; they consist of unilateral or bilateral small bony protu- material while the core remains ligamentous, resulting in a
berance at the anterior boundary of the foramen magnum. It is tube-like development instead of spur [7].
believed that their pathogenesis is derived from remnants of
the lateral hypochordal blastema of the proatlas. In rare occur- Arterial supply and venous relationships
rences, the larger basilar processes communicate with the an-
terior arch of the atlas resulting in instability of the The arterial supply of the clivus (Fig. 10) is primarily derived
atlantooccipital joint [7]. If the hypochordal blastema of the from two vessels. The first is a branch off the internal carotid
proatlas persisted in the medial aspect, it would give rise to a artery, the meningohypophyseal trunk, and the second main
third condyle at the anterior margin of the foramen magnum vessel is a branch of the ascending pharyngeal artery, the pos-
[16]. A much scarcer variant is the arcus praebasioccipitalis terior meningeal artery [18]. There are many variations re-
occurring in 0.03% of the population. It is an osseous mass in garding the meningohypophyseal trunk in terms of its
the shape of a horseshoe positioned at the anterior margin of branching and anastomoses [25]. The meningohypophyseal
the foramen magnum formed by the complete persistence of trunk gives off the dorsal meningeal artery, which passes pos-
the hypochordal blastemas. It may affect the functioning of the teriorly through the cavernous sinus, within Dorello’s canal
craniovertebral joints. with the abducens nerve and the inferior petrosal sinus, to
The presences of bony canals through the clivus (Fig. 9) are supply the clival dura mater. Alongside the inferior petrosal
suggested to contain communicating vessels with the internal sinus runs the lateral clival artery, which anastomosis with the
and external venous plexus. When the basal segment of the posterior meningeal artery. The medial group of branches sup-
occipital canal contains a bony canal known as basilar canalis, plies the apex of the clivus to the height of where the abducens
it may carry a previous basivertebral veins originating from nerve emerges. A branch of the ascending pharyngeal artery,
the vertebral material integrated into the skull base. It is pres- the posterior meningeal artery, passes through the jugular fo-
ent among 8% of the population; however, the median basilar ramen and enters the posterior cranial fossa supplying the
canalis, which emerges from the midline of the basiocciput, inferior dura mater of the clivus [18]. The blood supply of
has a prevalence of 20% in newborns and is rarely seen in the clivus is clinically significant due to the implications of
adults, only 1%. The embryology of the basilar canals is tumors. Dorsal to the clivus, the basilar artery and basilar
Childs Nerv Syst

Fig. 10 Blood supply to the


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

venous plexus are found and can create faint grooves on the Neoplastic tumors
bone [3]. Since the original development of the basilar venous
plexus (Fig. 4) is related to the vertebral column, it is consid- Meningioma The dorsal dural surface of the clivus increases its
ered a constituent of Batson’s plexus [7]. propensity of being affected by meningiomas. Due to the lack of
arachnoid granulations at the central aspect of the clivus, menin-
Pathology giomas arise more commonly at the petroclival line. As a result,
meningiomas are often located medial to the trigeminal nerve [7,
Non-neoplastic tumors 20]. When excising the tumor, neurosurgeons must be attentive
toward the vasculature surrounding the mass.
Fibrous dysplasia Fibrous dysplasia is a benign skeletal anom-
aly that may affect one or multiple bones, with a greater ten- Chordomas Chordomas are similar to ecchordosis physaliphora
dency to affect long bones, ribs, and craniofacial bones [2]. in that they are both relics of notochordal tissue. The direction of
The mature bone becomes replaced with a weaker substitute travel of the notochord from the odontoid process moving ante-
of woven bone and fibrous tissue. More commonly, the disor- riorly toward the basiocciput can lead to susceptibility of noto-
der affects a single bone in 70% of cases and multiple bones in chord remnants within the area and lead to the development of
30% [1]. McCune-Albright syndrome involves multiple bone chordomas [24]. However, compared to ecchordosis
subtype of fibrous dysplasia, café-au-lait spots, and endocrine physaliphora, chordomas are malignant tumors arising within
disorders, in which the clivus and sphenoid bone may be in- the bone in a slow growing manner with a potential to metasta-
volved [14]. Imaging with a ground glass appearance is pa- size via lymphatics or hematogenously [7]. Chordomas are un-
thognomonic for fibrous dysplasia. common and account for less than 1% of all intracranial tumors
[24]. They have a greater prevalence in males by the third and
Neurenteric cyst If CT images display an integral cortex with fourth decades of life and commonly occur is the sacrum, clivus,
lytic lesions, it should raise concerns of a possible neurenteric and cervical vertebrae. Approximately one-third occur at the
cyst [7]. A location at the clivus is unusual but not surprising clivus originating within the bone as a well circumcised, midline
given that the embryological nature involves dysgenesis of the extradural soft-tissue mass and often affecting the abducens
notochord during early development [11]. nerve at initial presentation [5]. On imaging, clival chondromas
appear as soft tissue masses with lytic bone destruction. Due to
Ecchordosis physaliphora Ecchordosis physaliphora is a con- high fluid content of the chordomas, on T1-weighted MRI, they
genital hamartomatous lesion derived from notochord rem- appear hyperintense, while on T2-weighted MRI, they appear
nants and is seen in approximately 2% of the population. It hypotense (as opposed to ecchordosis physaliphora) with mod-
is located in the retroclival region and projects toward the erate degree of contrast enhancement [7]. Treating chordomas are
intradural prepontine cistern. The tissue appears hypotense difficult as they often recur and occupy a difficult location in
on T1-weighted MRI and hypertense on T2-weighted MRI terms of neighboring neurovascular structures. Clival chordomas
with a lack of contrast enhancement compared to other tumors sit in close proximity to the brain stem, thus compressive growth
such as chordomas. The clinical repercussion of this tumor- and inadequately managed tumors often lead to high morbidity
like mass is bleeding or CSF leakage [7]. and mortality [26].
Childs Nerv Syst

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