INCIDENCE OF ATLAS BRIDGES AND TUNNELS – THEIR PHYLOGENY , ONTOGENY AND CLINICAL IMPLICATIONS

Monika Lalit, Sanjay Piplani, Anterpreet K. Arora, Jagdey S. Kullar, Tripta Sharma Department of Anatomy, Sri Guru Ram Das Institute of Medical Sciences and Research, Amritsar, Punjab, India Department of Pathology, Sri Guru Ram Das Institute of Medical Sciences and Research, Amritsar, Punjab, India Department of Anatomy, Govt. Medical College, Amritsar, India Department of Anatomy, Punjab Institute of Medical sciences, Jalandhar, Punjab, India


INTRODUCTION
In human atlas vertebrae, the superior aspect of posterior arch of atlas is characterized by a groove known as sulcus arteriae vertebralis for the passage of vertebral artery and suboccipital nerve.The groove may be shallow, deep or at times, bony outgrowths known as atlas bridges may develop over this segment.These bridges may indicate anomalous ossification of the groove by oblique ligament of atlas; a fibrous tissue present at the lower border of posterior atlanto-occipital membrane converting the groove to form a complete or incomplete bony ring (William et al, 1995).The occurrence of this bony bridge has been well documented in the literature (Allen, 1879;Cleland, 1860) where it has been variously described as foramen sagittale atlantis, foramen atlantoideum posterior, kimmerle variant,foramen atlantoideum vertebrale, foramen retroarticulare superior, canalis arteriae vertebralis, arcuate foramen, retrocondylar vertebral artery ring, ponticulus posterior, retroarticular canal, pons ponticus, posterior glenoid process and speculum (Hasan et al, 2001).Ponticulus posticus (posterior bridge) and Ponticulus lateralis (lateral bridge) are the two kinds of bridges and sometimes a combination of these two for example ponticulus posterolateralis is also present.The posterior bridge is an osseous bridge that is formed between the posterior margin of superior articular facets and the posterior arch of the atlas and when complete forms the retroarticular canal.Whereas the lateral bridge is a lateral outgrowth of bone that bridges the lateral margin of the superior articular facets to posterior root of transverse process of the atlas and may exist as supra-transverse foramen.In ponticulus posterolateralis, a wide bony fragment extends from the lateral margin of posterior one third of superior articular facet to the transverse process and dorsal edge of the vertebral groove of the atlas (Mitchell, 1998a;Hasan et al, 2001).The vertebral artery is most vulnerable for compression during extreme rotation of head and neck movements presenting with dizziness fainting and transient diplopia.Occurrence of these bridges may further compromise the caliber of already stretched vertebral artery (Hasan et al, 2001).Cushing et al (2001) found an association between the arcuate foramen and tethering of vertebral artery in it, leading to its dissection from repetitive trauma with movement of neck.Tubbs et al (2007) emphasised that bony bridge forming arcuate foramen may cause external pressure on the vertebral artery as the later passes through it to the foramen magnum.Thus this anatomical variation of atlas bridging draws attention and may facilitate interpretation of radiological findings, guide certain neurosurgical interventions, note of caution when cranio-vertebral manifestations are carried out.

MATERIALS AND METHODS
A total of 60 (120 sides) complete dry human atlas vertebrae obtained from the skeletal collection from the Department of Anatomy, Government Medical College, Amritsar, Punjab.All the vertebrae were undamaged, thoroughly boiled, cleaned and numbered from 1-60 each.The posterior arch of atlas vertebrae was examined for the evidence of exostosis from posterior margin of superior articular facet and the specimens exhibiting such bony outgrowths were classified as having either a complete or incomplete bony ring.The morphology of atlas bridges i.e. posterior bridge, lateral bridge and posterolateral tunnels was studied and observations thus were made on the variability of sulcus/canalis arteriae vertebralis for example vertebral arterial grooves on all the atlas vertebrae following the criteria used by Mitchell (1998a) and Hasan et al (2001) and statistical analysis was also done.According to Mitchell (1998a, b)
One (1.66%) postero-latetal tunnel was also observed on the left side (Figure 4).The difference in the localisation of the different types of bony outgrowths on right, left and bilateral sides was determined using Chi-Square test (χ 2 ), Degree of freedom (df) and p-value which was found to be x2=16.937;df=10; p=0.076;Not significant.(1972) that the lateral bridge develops from the material of lateral extension of proatlas and consequently belongs to manifestations of the occipital vertebra.It is also hypothesized that incomplete retroarticular canal is the precursor of complete bony ring (Paraskevas and Papaziogas, 2005).This opinion has also been supported by Kendrick and Biggs (1963) who after an observation of two females with a unilateral incomplete bony ring found a developing unilateral radio-opaque complete ring over a period of 1 to 2 years.The incidence of complete and incomplete posterior and lateral bridges is depicted in Table 1.Table 2 depicts the comparison of atlas bridges with Mitchell (1998) who gave 3 classes of atlas vertebrae based upon degree of formation of posterior and lateral bridges for the passage of third part of vertebral artery.In the present study, the left only type of complete bony ring has a higher incidence as compared to the right side in North Indians (Mitchell, 1998a).Mitchell (1998b) also worked on 147 samples of atlas vertebrae with lateral bridges but in our study no bilateral incomplete or complete lateral bridge was observed (Mitchell, 1998b).The number of lateral bridges occurring with retro-articular canal appears to increase with age after 40 years as a result of degenerative changes (Taitz and Nathan, 1986).2001) also worked extensively on the subject and classified the atlas bridges in 6 classes as shown in Table 3.As depicted from the table 3 the vertebral artery ring of atlas in the present study was compared on the basis of study of Hasan et al (2001) and the most common was found to be the impression for vertebral artery.No bilateral lateral ponticuli were seen and only one partial postero-lateral tunnel was observed on the left side only.The difference in the localisation of the different types of bony outgrowths on right, left and bilateral sides was found to be statistically insignificant.(x2=16.937;df=10; p=0.076).

DISCUSSION
Our findings that bilateral retroarticular canal has the lowest incidence, the right type of retroarticular canal having an incidence of 5 % and left only type having higher incidence 8.33% and 3.33% bilateral type in our North Indian samples.These conclusions support the findings of Lamberty and Zivanovic (1973) who found bilateral type having the lowest incidence 3.3% and the left only type the highest incidence in a skeletal sample of 60 American whites.Our findings also concurs with the Paraskevas and Papaziogas (2005) who also found that bilateral bony canal has the lowest incidence 1.13%, the right only type of bony ring having an incidence of 2.84% and the left only type the higher incidence 5.11% in Northern Greek skeletal sample.The phenomenon of higher occurrence of left only type than the right only type can be attributed to the explanation due in part to unequal weight bearing as a result of more commonly left tilted head posture (Dhall et al, 1993).Owing to the right sided dominance of muscles of the body in right handers, the larger and consequently stronger sternocleidomastoid muscle would tend to tilt the head towards opposite side (Pande and Singh, 1971).It is also believed that atlas bridges are more common in individuals who sustain greater stress in the region of cranio-cervical junction (Taitz and Nathan, 1986).
In the present study the lateral bridges and postero-lateral tunnels were more commonly observed on the left side.These findings support the findings of Dhall et al (1993) who also observed an increased incidence of bridges on the left side and correlated with the larger superior articular facets on that side (Hasan et al, 2001).According to Macalister (1869) a variable tongue shaped outgrowth known as postglenoid process arises from the hinder and outer lip of glenoid cavity which is present in 21% of the atlas vertebrae in some degree, becomes ossified and sometimes sufficiently large to convert that groove into a foramen forming a bridge over the vertebral artery and suboccipital nerve.Thus this bridge is chiefly formed by the extension of ossification into ligament from the post-glenoid end, where it is incomplete behind.
In the evolutionay history in primates, the prevalence of both types of bridges is very high in non-hominoids primates whereas it is relatively low in extant hominoids and hominoids and even lower in humans.This trend appears to correspond to postural changes in primates from quadrupedalism where head is supported by extensor muscles of neck and ligaments to bipedalism for example in man, where weight of head is borne by vertical loading of SAF of atlas and roof of the tunnel thus has disappeared.It is reported that the posterior bridge occurs in various mammals like chiropetra, carnivore, cetacean, pinnipedia, edentate artiodactyla (Le Double, 1912).However, almost all cases of Japanese macaques have a bilateral complete posterior bridge the development of which is demonstrated to be a normal process of growth.
The lateral bridge starts to form later and more gradually than the posterior bridge (Yamamoto, 2006).However, the true oblique process is of common occurrence in monkey, bear, lion, leopard, sheep, deer and goat, etc (Macalister, 1869).High incidence of this bony ring suggests that it may be of significance in aetiology of vertebrobasilar insufficiency presenting with dizziness, fainting and transient diplopia as many cases have been reported where surgical removal of bony bridges alleviate the symptoms of vertebrobasilar insufficiency (Taitz and Nathan, 1978).Ercegovac and Davidovic (1970) , 1999).
In an individual with a lateral bridge of atlas and an associated retroarticular canal may further results in increased compression of the vertebral artery and compromised blood flow during extreme rotation of head and neck as occurs in manipulation of cervical spine (Parkin et al, 1978).Hence knowledge of quantitative anatomy of the vertebral artery groove will prove useful to surgeons performing operative procedures in this region and help in avoiding vascular complications.
there are 3 classes of posterior bridge as: Class I -Groove of vertebral artery, Class II -Retroarticular sulcus showing incomplete ring with middle part missing which is formed by exostosis (bony lipping) of posterior border of lateral mass and posterior arch of atlas, Class III -Retroarticular canal showing a complete bony ring enclosing the vertebral artery.Lateral bridge shows complete ring incomplete rings According to Hasan et al (2001) there are 6 classes as: Class I -only the impression of vertebral artery on posterior arch of atlas, Class IIwhen this impression becomes deeper then becomes groove i.e.Deep groove for vertebral artery, Class III -Partial posterior ponticulus as a bony spicule extending from the superior articular facet overhanging the dorsal arch, Class IV -Complete posterior ponticulus, Class V -Partial lateral ponticulus extended from the lateral mass to the transverse process, Class VI -Partial posterolateral tunnel

Figure 2A -Figure 2B -
Figure 2A-Left partial posterior ponticulus (noted as A bony spicule extending from the superior articular facet (SAF) overhanging the posterior arch of atlas).SAF-Superior Articular Facet, P-Posterior Arch, AA-Anterior Arch Origin of bridges (posterior and lateral bridgeand postero-lateral tunnels) is a matter of much debate and different workers have put forward many theories for their s Atlas tunnels and bridges Rev Arg de Anat Clin; 2014, 6 (1): 26-34 __________________________________________________________________________________________ Todos los derechos reservados.Reg.Nº: 5104953 www.anatclinar.com.ardevelopment.The posterior bridge (retroarticular ring) was first reported by Macalister (1869).Later on its detailed morphology was studied by Macalister (1893) and Le Double (1912) and has drawn attention of many anatomists since then.

Figure
Figure 4A, B.-Superior view (a) and superolateral view (b) of atlas showing partial posterolateral tunnel as a combination of incomplete posterior and lateral bridges.Tr-Transverse process, SAF-Superior articular facet, A-Anterior arch, P-Posterior arch

Table 3 -
Comparision of atlas bridges with hasan et al, 2001 Todos los derechos reservados.Reg.Nº: 5104953 www.anatclinar.com.arHasan et al ( Cakmak et al (2005)4)ms of vertebrobasilar insufficiency by surgical removal of bony ring in eight cases.Cacciola et al (2004)while elaborating it further revealed that the vertebral artery occupies 57% of the vertebral artery groove over the lateral part of the posterior arch of atlas.When a foramen is formed over here, it produces a relatively tight situation of vertebral artery leading to giddiness on external neck movements due to vertebrabasilar insufficiency.Cakmak et al (2005)asserted that cervical spine radiography is a simple and useful technique to know the presence of arcuate foramen and should be considered if a patient comes with symptoms like pain in temporal region, pain in back of eye, vertigo, occipital headache, periodic photophobia, paresthesia of hands or sensation of pressure on hands.Moreover whiplash injuries a type of neck hyperflexion are very common nowadays, occurring during traffic accidents that may lead to rupture of the ligaments and posterior atlantooccipital membrane resulting in ossification Atlas tunnels and bridges Rev Arg de Anat Clin; 2014, 6 (1): 26-34 __________________________________________________________________________________________ Todos los derechos reservados.Reg.Nº: 5104953 www.anatclinar.com.arprocedure due to deposition of calcium salts in the formed haematoma at the rupture sites (McRae