THE INCIDENCE OF ATLANTO-OCCIPITALIZATION AND ADDITIONAL FORAMINA PRESENT IN THE DRY SKULLS OF NEPALESE POPULATION

1* 2 3 Rubina Shakya , Nirju Ranjit , Shamsher Shrestha


INTRODUCTION
Occipitalisa on of Atlas or the atlanto-occipital fusion is one of the skeletal varia ons where the adjacent part of the basiocciput gets fused with its succeeding first cervical vertebra (Atlas). In a normal skull, lateral masses of the atlas form ellipsoid synovial ar cula ons with the occipital condyles. Since it is a biaxial joint, two movements are possible; one, around the transverse axis and the other, 1 around the antero-posterior axis. If there is the occurrence of atlanto-occipital assimila on, then there will be no existence of the aforemen oned movements. Rather, it leads to atlanto-axial hypermobility and has been reported to be associated with atlanto-axial subluxa on, basilar i nva g i n a o n , K l i p p e l Fe i l Sy n d ro m e , a n d C h i a r i 2-3 malforma on. The basi-occiput and occipital condyles are developed from the caudal half of the fourth occipital sclerotome and the cranial half of the first cervical sclerotome. Whereas, the atlas or the first cervical vertebra is developed from the caudal half of the first cervical sclerotome and the cranial half of the second cervical sclerotome. During the fourth week of the embryonic period, the adjoining parts of sclerotomes proliferate so extensively that they get incorporated into each other, giving rise to an individual vertebra. However, the mesenchymal ssue lying intermediate to cranial and caudal parts of each sclerotome do not proliferate which eventually gets segmented by the 4 development of intervertebral disc. The failure of segmenta on between the cranial and caudal parts of the first cervical sclerotome leads to the AOZ since it gets assimilated with its preceding fourth occipital sclerotome. 5 6 The fusion could be par al or complete, which might cause a major risk in neurovascular injury during the surgical interven on. In such cases, very careful examina on is th required in regard to the 4 part of the vertebral artery and the first cervical nerve. Besides, it also reduces the diameter 5 of the foramen magnum that might cause compression in 7 the spinomedullary region leading to neurological deficits. Knowledge of the normal ossifica on pa erns is also necessary to find the variant cle or foramina present in the 8 skull.
Thus, we aimed to inves gate the incidence of occipitaliza on of Atlas and related variant foramina, as the baseline awareness of these condi ons among the Nepalese popula on.

METHODOLOGY
The total 86 dry skulls were examined from the collec on maintained in the department of Anatomy in Kathmandu University of Medical Sciences, Ins tute of Medical Science, and B.P. Koirala Ins tute of Health Sciences. This retrospec ve study was conducted during the period extending from Jan 2020 to March 2021. The skulls were examined thoroughly in order to iden fy the occurrence of cranio-vertebral varia ons. The degree (par al or complete) and the side of assimila on (unilateral or bilateral) were examined in the case of Atlanto-occipitaliza on.The anteroposterior (AP) and transverse (T) diameters of the foramen magnum (FM) were measured with the help of Vernier caliper. AP and T diameters of FM were measured as the maximum internal length along the midsagi al plane and the maximum internal width perpendicular to the midsagi al plane, respec vely. These data were evaluated with the descrip ve sta s cs using SPSS so ware version-25.Furthermore, the presence of cranial variant foramina was confirmed by inser ng syringe-needle or probe through it.

RESULTS
Out of 86 adult human dry skulls, two cases (2.3 %) were found with the par al atlanto-occipitaliza on (AOZ). In both of the cases, AOZ was accompanied by the posterior spina bifida, close to the midline ( Fig. 1-2). Lateral masses of the atlas were fused with the occipital condyles. One of those AOZ skulls presented a fusion of the right lateral mass of the posterior neural arch (

DISCUSSION
Since the atlanto-occipitaliza on (AOZ) is associated with many other craniovertebral anomalies and the neurovascular pathology, the knowledge of its incidence is required to an cipate the clinical manifesta on and their possible treatments. This study found the incidence of par al AOZ to be 2.3 % (2 out of 86 skulls) in Nepalese popula on ( Fig.1-2). The review of it in the different 5,[9][10][11][12] popula ons ranges from 0.3 to 3.63 % (Table 1), the 11 10 lowest in Thai, and the highest in Malaysian popula ons. The AOZ is caused bythe failure of segmenta on between the cranial and caudal parts of first cervical sclerotome resul ng the assimila on of the first cervical vertebra (the atlas) into the basicranium. It o en leads to having the anomalous course of the vertebral artery that has to be seriously taken care of, during surgical procedures on the craniovertebral junc on, hence, it requires well pre-procedural planning with the help of computed tomographic angiography. In 78.4% cases of AOZ, the course of vertebral artery has been found passing through a bony canal between the fused part of the atlas and basicranium, whereas in 13 20.3% cases, passing below the atlas. The immobility of atlanto-occipital joint, on the other hand, causes hypermobility of lateral atlantoaxial joints and could overstress the transverse ligament which may lead to the   Both cases of the AOZ were accompanied by the presence of spina bifida approximately at the midline ( Fig.1-2). The case of only spina bifida usually remains asymptoma c unless there is any impingement on the surrounding structure including the spinal cord and vertebral artery. Such case of defect limited to the bone, seemingly normal as it is covered by the skin, is known as spina bifida occulta (SBO). Some mes, the indica ons are visible on the newborn's skin showing 16 abnormal tu of hair or a small dimple. The SBO in Atlas is caused by the persistence of posterior midline synchondrosis between the two primary ossifica on centers of the [17][18][19] posterior neural arch. The incomplete fusion of these ossifica on centers at the midline of the posterior neural 20 arch may be normal for the age of 5-10 years. The study on normal ossifica on pa ern of Atlas showed that the complete fusion of ossifica on centers of the posterior neural arch occur at the average age of 5 years (age range 2- 17 13 years). Some cases of atlas-SBO in the adults were found symptoma c of the cervicogenic headache (CEH) with the pain intensity; moderate (16 cases) and intense (1 case) out of 17 cases. In such cases, pain remission was observed a er 21 the blockade of the greater occipital nerve. However, there is a dispute regarding the atlas-SBO induced bilateral headache since many authors have described the [22][23] unilaterality of the pain in the CEH.
Apart from AOZ, some congenital anomalies of cranial base are associated with the presence of addi onal structures and foramina that holds the interest for clinicians where neurosurgical and vascular approach is a requisite. During embryogenesis, the car laginous precursors make its appearance to form the ala temporalis (future greater wing) from paraxial mesoderm, further growth of which, gets extended surrounding the nerves and vessels, crea ng the specific foramina for them. Some mes, minor varia ons may take place resul ng in the addi onal foramina, for e.g. 'Sphenoidal emissary foramen (SEF)' or 'Foramen of Vesalius'. It is believed that the SEF represents the site of fusion between, anteriorly ala orbitalis-membranous part, [24][25][26] and medially ala temporalis-car laginous part. The present study found the case of unilateral SEF in 19.7% (17/86) skulls which seems to be a quite high incidence rate as compared to AOZ (2.3%, 2/86). But, our finding of SEF looks more or less concomitant to the data of previous 27 studies in the Japanese (21.75%) and the Turkish (28.1%, 28 81/317) popula on. It has been found even higher in other 25,[29][30][31] popula ons ranging from 40 -80% (Table 3), sugges ng it as a common varia on. However, its existence and considera on may help for the safer percutaneous approach to the middle cranial fossa through the foramen ovale, which could be mistaken with the SEF. Since it gives passage to a large emissary vein connec ng the pterygoid plexus 32 with cavernous sinus , may cause profuse intracranial bleeding in case of its existen al negligence. This study also found one interes ng case of complete pterygospinousbar among 86 skulls (1.1%) present unilaterally on the le side. It is formed by the mineraliza on of pterygospinous (Civinini) ligament which is a thickening of interpterygoid aponeurosis, extending from the base of the spine of sphenoid to the posterior border of the lateral pterygoid plate. The published rate of pterygospinous complete mineraliza on is variable in different popula on [33][34][35][36][37] with the range of 1.1 -8.61% (Table 4). This bony bar is definitely a significant obstacle for neurosurgeons while approaching the retropharyngeal and parapharygeal 38,39 space.
The complete mineraliza on of this ligament results in the forma on of an addi onal foramen superiorly, 'pterygospinous foramen' or 'foramen of Civinini' (Fig.3B), very close to the foramen ovale, and giving passage to some branches of the mandibular nerve. In par cular, lingual and inferior alveolar branches of the mandibular nerve may get compressed during the contrac on of pterygoid muscles, 40 developing a trigeminal neuralgia.

CONCLUSION
The incidence of atlanto-occipitaliza on and pterygospinous bar seems to be quite low as compared to presence of an addi onal sphenoidal emissary foramen. The occurrence of craniovertebral synostosis and structural varia ons in cranial base, in terms of addi onal structures and foramina, bears a huge significance from clinical aspects. Hence, documenta on of these varia ons among the Nepalese popula on, may contribute to prognos c implica ons, safer approach on surgery, or, broaden its therapeu c approach.

LIMITATION OF THE STUDY
Even though the dry skulls with the complete closure of fontanelles and completely ossified bones were considered in this study, there was no record of the exact age and gender.