gross morphology of the bridges over the vertebral artery groove on the atlas

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ORIGINAL ARTICLE George Paraskevas Basilios Papaziogas Christos Tsonidis George Kapetanos Gross morphology of the bridges over the vertebral artery groove on the atlas Received: 21 April 2004 / Accepted: 18 June 2004 / Published online: 31 March 2005 Ó Springer-Verlag 2005 Abstract The bony bridges of the atlas over the ‘‘groove of the vertebral artery’’ are commonly seen in plain radiographs of the cervical spine, and it is a subject of controversy whether they cause compression of the underneath lying vertebral artery. To clarify this we examined a total of 176 dried and complete atlas verte- brae and found the presence of a ‘‘canal for the vertebral artery’’ (CVA) in 10.23% and an incomplete ‘‘canal for the vertebral artery’’ in 24.43%. The CVA and incom- plete CVA is more common in males (11.11% and 24.9%) than in females (9.3% and 24.42%). We found a higher incidence of CVA in laborers (37.5%) than in nonlaborers (4.16%). The incomplete CVA appeared to be more characteristic in the age group of 5–44 years. In the age group of 45–90 years the CVA was characteris- tic, which probably means that an incomplete CVA is the precursor of a CVA. The superoinferior diameter of the CVA canal ranged from 5.1 to 6.1 mm at the right side and from 4.6 to 5.8 mm at the left side, while the anteroposterior diameter was 5.6–6.9 mm at the right side and 6.1–7.2 mm at the left side. We also found a high incidence of coexistence of CVA and the ‘‘retro- transverse foramen’’ (72.22%) which means that because of possible compression of the vertebral veins the blood flow is directed into the small vein of the retrotransverse foramen. Finally, in 93.5% of unilateral CVA a deeply excavated contralateral ‘‘groove of the vertebral artery’’ was found. Keywords Atlas Groove of vertebral artery Bridges Introduction It has been noted that the ‘‘groove of the vertebral ar- tery’’ which lies behind the superior articular surface may be shallow, or deep, or bridged by a bony ring either placed laterally in relation to the previous surface or posteriorly to it, the latter forming the so-called ‘‘canal for the vertebral artery’’ (CVA) [10]. In addition, the CVA may be incomplete, and sometimes a combi- nation of the posterior and lateral bridge is present. The presence of the posterior bridge, i.e., the CVA, is well documented in the literature [6, 14, 20, 23, 29, 30]. In general anatomical textbooks it is reported that occa- sionally the ‘‘groove of the vertebral artery’’ is converted into the CVA by an ossification in the fibrous tissue that bridges it [26, 35]. The bony fragment that bridges the ‘‘groove of the vertebral artery’’ extending from the lateral mass of the atlas to the posteromedial margin of the sulcus is called a ‘‘ponticulus posterior’’ [16]. For this fragment we propose the term ‘‘posterior bridge.’’ This bony fragment may be completely present CVA or may consist of small tips (incomplete CVA). In cases in which a CVA is formed by the bony bridge this canal has been called ‘‘Kimmerle’s variant’’ [13], ‘‘superior retroarticu- lar foramen’’ [4], ‘‘foramen arcuale’’ [33], ‘‘foramen at- lantoideum posterius’’ [3], ‘‘foramen sagittale atlantis’’ [17], ‘‘foramen atlantoideum vertebrae’’ [8] ‘‘retroc- ondylar vertebral artery ring’’ [14], ‘‘canalis arteriae vertebralis’’ [36], ‘‘retroarticular canal’’ [20], and ‘‘atlas bridging’’ [30]. The CVA represents a frequent abnormality, and its incidence, according various authors, is 11.7% [15], 7.4% [17], 10% [11], 18% [32], 7.9% [30], 11% [22], 9.8% [20], 21% [24], and 15% [14]. According to Taitz et al. [30] the incidence of an incomplete CVA is 25.9%, while Radojevic et al. [24] found an incidence of 2%, Lamberty et al. [14] 21.66%, and Mitchell [20] 29.6%. G. Paraskevas (&) B. Papaziogas Department of Anatomy, Faculty of Medicine, Aristotle University of Salonica, Salonica, Greece E-mail: [email protected] Tel.: +30-2310-999361 Fax: +30-2310-992563 C. Tsonidis 2nd Neurosurgical Clinic, Faculty of Medicine, Aristotle University of Salonica, Salonica, Greece G. Kapetanos 3rd Orthopaedic Clinic, Faculty of Medicine, Aristotle University of Salonica, Salonica, Greece Surg Radiol Anat (2005) 27: 129–136 DOI 10.1007/s00276-004-0300-9

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Page 1: Gross morphology of the bridges over the vertebral artery groove on the atlas

ORIGINAL ARTICLE

George Paraskevas Æ Basilios PapaziogasChristos Tsonidis Æ George Kapetanos

Gross morphology of the bridges over the vertebral arterygroove on the atlas

Received: 21 April 2004 / Accepted: 18 June 2004 / Published online: 31 March 2005� Springer-Verlag 2005

Abstract The bony bridges of the atlas over the ‘‘grooveof the vertebral artery’’ are commonly seen in plainradiographs of the cervical spine, and it is a subject ofcontroversy whether they cause compression of theunderneath lying vertebral artery. To clarify this weexamined a total of 176 dried and complete atlas verte-brae and found the presence of a ‘‘canal for the vertebralartery’’ (CVA) in 10.23% and an incomplete ‘‘canal forthe vertebral artery’’ in 24.43%. The CVA and incom-plete CVA is more common in males (11.11% and24.9%) than in females (9.3% and 24.42%). We found ahigher incidence of CVA in laborers (37.5%) than innonlaborers (4.16%). The incomplete CVA appeared tobe more characteristic in the age group of 5–44 years. Inthe age group of 45–90 years the CVA was characteris-tic, which probably means that an incomplete CVA isthe precursor of a CVA. The superoinferior diameter ofthe CVA canal ranged from 5.1 to 6.1 mm at the rightside and from 4.6 to 5.8 mm at the left side, while theanteroposterior diameter was 5.6–6.9 mm at the rightside and 6.1–7.2 mm at the left side. We also found ahigh incidence of coexistence of CVA and the ‘‘retro-transverse foramen’’ (72.22%) which means that becauseof possible compression of the vertebral veins the bloodflow is directed into the small vein of the retrotransverseforamen. Finally, in 93.5% of unilateral CVA a deeplyexcavated contralateral ‘‘groove of the vertebral artery’’was found.

Keywords Atlas Æ Groove of vertebral artery Æ Bridges

Introduction

It has been noted that the ‘‘groove of the vertebral ar-tery’’ which lies behind the superior articular surfacemay be shallow, or deep, or bridged by a bony ringeither placed laterally in relation to the previous surfaceor posteriorly to it, the latter forming the so-called‘‘canal for the vertebral artery’’ (CVA) [10]. In addition,the CVA may be incomplete, and sometimes a combi-nation of the posterior and lateral bridge is present. Thepresence of the posterior bridge, i.e., the CVA, is welldocumented in the literature [6, 14, 20, 23, 29, 30]. Ingeneral anatomical textbooks it is reported that occa-sionally the ‘‘groove of the vertebral artery’’ is convertedinto the CVA by an ossification in the fibrous tissue thatbridges it [26, 35]. The bony fragment that bridges the‘‘groove of the vertebral artery’’ extending from thelateral mass of the atlas to the posteromedial margin ofthe sulcus is called a ‘‘ponticulus posterior’’ [16]. For thisfragment we propose the term ‘‘posterior bridge.’’ Thisbony fragment may be completely present CVA or mayconsist of small tips (incomplete CVA). In cases in whicha CVA is formed by the bony bridge this canal has beencalled ‘‘Kimmerle’s variant’’ [13], ‘‘superior retroarticu-lar foramen’’ [4], ‘‘foramen arcuale’’ [33], ‘‘foramen at-lantoideum posterius’’ [3], ‘‘foramen sagittale atlantis’’[17], ‘‘foramen atlantoideum vertebrae’’ [8] ‘‘retroc-ondylar vertebral artery ring’’ [14], ‘‘canalis arteriaevertebralis’’ [36], ‘‘retroarticular canal’’ [20], and ‘‘atlasbridging’’ [30].

The CVA represents a frequent abnormality, and itsincidence, according various authors, is 11.7% [15],7.4% [17], 10% [11], 18% [32], 7.9% [30], 11% [22],9.8% [20], 21% [24], and 15% [14]. According to Taitzet al. [30] the incidence of an incomplete CVA is 25.9%,while Radojevic et al. [24] found an incidence of 2%,Lamberty et al. [14] 21.66%, and Mitchell [20] 29.6%.

G. Paraskevas (&) Æ B. PapaziogasDepartment of Anatomy, Faculty of Medicine,Aristotle University of Salonica, Salonica, GreeceE-mail: [email protected].: +30-2310-999361Fax: +30-2310-992563

C. Tsonidis2nd Neurosurgical Clinic, Faculty of Medicine,Aristotle University of Salonica, Salonica, Greece

G. Kapetanos3rd Orthopaedic Clinic, Faculty of Medicine,Aristotle University of Salonica, Salonica, Greece

Surg Radiol Anat (2005) 27: 129–136DOI 10.1007/s00276-004-0300-9

Page 2: Gross morphology of the bridges over the vertebral artery groove on the atlas

Studying radiographs of the cervical spine taken atrandom Radojevic et al. [24] saw the CVA in 3.4% of thecases and incomplete CVA in 1%, while Lamberty et al.[14] saw the CVA in 7.58% of the cases and incompleteCVA in 6.06%.

The presence of a lateral bony bridge at the atlascalled the ‘‘ponticulus lateralis’’ is less frequent than the‘‘ponticulus posterior’’ [16]; for that bony bridge wepropose the term ‘‘lateral bridge.’’ That bridge extendsfrom the upper edge of the lateral mass to the lateral tipof the transverse process, covering the vertebral artery.Le Double [15] reported an incidence of 1.8%, Barge [2]2.3%, Hayek [11] 2.9%, Toro et al. [32] 3.5%, Radojevicet al. [24] 2.5%, and Taitz et al. [30] 3.8%. The ‘‘lateralbridge,’’ as has been reported previously, occurs veryrarely in any literature due to the difficulty with identi-fication on anteroposterior and lateral radiographs.Occasionally cases have been reported in which a widebony fragment extends from the lateral margin of theposterior third of the superior articular facet to thetransverse process and dorsal edge of the vertebralgroove of the atlas. This type of bridging of the vertebralartery is a combination of a ‘‘ponticulus posterior’’ witha ‘‘ponticulus lateralis.’’ The proposed name of thisbridge by Prescher [22] is ‘‘ponticulus posterolateralis,’’and the reported incidence by the same author in a seriesof 200 atlases was 1.5%. We propose, as an official term,the ‘‘posterolateral bridge’’ of the atlas. Additionally, asmall or large foramen may exist as a passage for theoccipital nerve and small vein, this foramen being lo-cated at the upper portion of the ‘‘posterolateralbridge.’’

The bony bridges of the atlas are common structuresin other vertebrates [15]. The origin of the bridges is asubject of much debate. Previous authors contributedthe formation of the ‘‘posterior bridge’’ to the persis-tence of the superior oblique process of other mammals[1, 18]. Other authors [9, 34] are convinced that the‘‘posterior bridge’’ is a late ossification of the lateral fi-bers of the posterior atlanto-occipital membrane. LeDouble [15] claimed that the ‘‘posterior bridge’’ repre-sents an acquired ossification of ligaments induced bythe pulsation of the vertebral artery, while Barge [2]believed that an activation of a special osteogeneticpotency exists in the region of the craniocervical junc-tion. Rambaud et al. [25] and Lamberty et al. [14] con-sider the latter opinion be incorrect since cartilaginous‘‘posterior bridges’’ have been seen in fetuses and chil-dren. Von Torklus et al. [33] had regarded both the‘‘posterior and lateral bridges’’ as representing an‘‘occipital vertebra.’’ This opinion concurs with thestatement of Burlet [5] that the ‘‘posterior bridge’’develops from material of the dorsal arch of the proatlasand belongs definitely to the manifestations of theoccipital vertebra. Saunders [27] and Selby et al. [28]believe that the ‘‘posterior bridge’’ has a substantialgenetic basis and is therefore familial in nature. For the‘‘lateral bridge,’’ according to Hayek [11], this bridgedevelops from material of the lateral extension of the

proatlas which also forms the complex of variants of theparacondylic process and consequently clearly belongsto the manifestations of the occipital vertebra.

The presence of the formed CVA is a structure whoseclinical significance and description have not yet beenfully understood. The existence of CVA may cause acompression effect on the vertebral artery as it crossesthe posterior arch of the atlas during extremes in therange of rotational movements of the head and neck [14,30]. The aim of our study was mainly to describe ana-lytically the morphological features of these bridges andthe possible relationship with other variants of the atlasand to make suggestions for the possible obstruction ofthe vertebral artery through an examination of dryspecimens.

Material and methods

The ‘‘groove of the vertebral artery’’ of the atlas, and themorphology of the bridges arising from the posterioredge of the superior articular surface, posteriorly andlaterally was studied in a total of 176 complete and freeof pathological features atlas vertebrae which were ob-tained from the skeletal collection of the Department ofAnatomy, Faculty of Medicine, Aristotle University ofSalonica, and from the personal osteology collection ofone of the authors (G.P.). The study took place at theLaboratory of Morphometric Analysis. All the speci-mens of the present study were of known sex and age,ranging from 5 to 90 years. The examined specimenscorrespond to the population of northern Greece, thuswhite race. We classified our specimens as ‘‘laborers’’ forthe cadavers of individuals with heavy and harmfulemployment and farmers and as ‘‘nonlaborers’’ for thecadavers of persons with higher education.

The posterior arches of the 176 atlases were examinedfor the presence of CVA and incomplete CVA located atthe posterior edge of the superior articular facet of theatlases. We studied the morphology of the CVA andincomplete CVA and the possible coexistence of the‘‘retrotransverse foramen’’ of the atlases, which is abony bridge extending from the posterior root of thetransverse process to the root of the posterior arch ofthe atlas. In addition, we examined the morphology ofthe ‘‘groove of vertebral artery’’ in comparison to theother side, where a CVA or incomplete CVA existed. Wealso referred to the bilateral type, right type, and lefttype of the CVA formed by a complete bridge of atlas.The CVA of the atlas vertebrae were measured with theaid of Vernier callipers interfaced with a standardcomputer. In particular, we measured the superoinferiorand the anteroposterior diameters of the CVA. All thesemeasurements were made from the lateral view of thecanals, while three atlases were excluded because of thepresence of exostosis.

Statistical analysis was performed with the t test.Statistical significance was set at P<0.05.

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Results

In our series of 176 specimens we found the presence of aCVA in 10.23% (Fig. 1) and an incomplete CVA in24.43% of the cases (Fig. 2). The CVA is located at themost lateral part of the posterior aspect of the lateralmass. The distribution of CVA and incomplete CVAaccording to sex is presented in Table 1. In studying thistable we conclude that the CVA and incomplete CVAare more common in males (11.11% and 24.4%respectively) than in females (9.3% and 24.42% respec-tively). From these results, in which the difference be-tween the two sexes is statistically nonsignificant, onemay consider that a minimal effect of gender on the atlasbridging may occur.

Also, the incidence of CVA and incomplete CVAaccording to the occupation (laborers and nonlaborers)is shown in Table 2. According to this table there is ahigher incidence of CVA (37.5%) in laborers than incomparison nonlaborers (4.16%). In addition, the inci-dence of incomplete CVA in laborers (50%) is signifi-cantly higher than that in nonlaborers (18.75%). Fromthese measurements one might conclude that someexternal factors, such as the custom of carrying heavyitems on the head could lead to the formation of theCVA.

The distribution of the atlas bridging according toage is shown in Fig. 3. From the study of this figure wefound that the incidence of incomplete CVA is higher inthe following age groups of 5–24 and 25–44 years(27.3% and 26.2%, respectively) and lower in age

groups 45–64 and 65–90 years (23.5% and 20.72%,respectively). In the age groups 45–64 and 65–90 yearsthe CVA is more characteristic (10.1% and 12.82%,respectively) than in age groups 5–24 and 25–44 years(8.9% and 9.1%, respectively). These results couldindicate that an ossification process takes place.

We noted that the form of incomplete CVA found inall cases is the absence of the middle part of the bridge,with the upper end most frequent (94.32%) in tubercleform and in the remainder of the samples (5.6%) inspine form, while in all the studied cases the lower endwas replaced by a small spine (Fig. 4).

Figure 5 shows the incidence of the CVA, having thelatter one occurring bilaterally on the right side only andon the left side only in the total sample. The bilateraltype of the CVA has the lowest incidence (1.13%) fol-lowed by the right-only type (2.84%) and the left-onlytype (5.11%). In particular the left-only type of CVA hasthe higher incidence in the four age groups (5.27%,5.32%, 4.98%, and 4.87%, respectively) while thebilateral type has the lowest incidence in these agegroups (1.29%, 1.05%, 1.12%, and 1.08%, respectively).We also concluded that in cases of left-only type andright-only type of CVA the contralateral ‘‘groove of thevertebral artery’’ was in 93.5% of cases deeply excavated(Fig. 6). This could be explained by the possible dilata-tion of the contralateral vertebral artery produced byipsilateral compression of the artery within the CVA.

The dimensions of the CVA in males, females, andthe overall sample are shown in Table 3. The two mea-sured dimensions, i.e., the superoinferior and the ante-roposterior diameter differed significantly (P<0.05). Inaddition, in measuring the above parameters on the leftand the right side there was no statistically significantdifference in the overall sample between age groups. Therange of superoinferior diameter of the CVA in theoverall sample was 5.1–6.1 mm at the right side (mean5.4±0.5 mm) and 4.6–5.8 mm at the left side (mean5.3±0.5 mm) while the range of the posteroinferiordiameter of the CVA was 5.6–6.9 mm at the right side

Fig. 1 Canal for the vertebral artery (CVA). a Location at the leftside. b Location at the right side, superior view of atlases

Fig. 2 Incomplete canal for the vertebral artery

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(mean 6.4±0.7 mm) and 6.1–7.2 mm at the left side(mean 6.7±0.3 mm). It is clear that the superoinferiordiameter is smaller than the anteroposterior, meaningthat in the case of a large vertebral artery the latter couldbe compressed superoinferiorly from the CVA.

Of the 176 atlas vertebrae examined we noted thepresence of the ‘‘lateral bridge’’ in 1.136% of the cases(Fig. 7). The ‘‘lateral bridge’’ extends from the upperedge of the lateral mass to the lateral tip of the trans-verse process. All of the studied cases were of unilaterallateral bridge. We also noted the presence of the ‘‘pos-terolateral bridge,’’ which extended from the lateralmargin of the posterior third of the superior articularfacet to the transverse process and dorsal edge of thevertebral groove, in 1.7% of the studied cases (Fig. 8).In all of these cases there was a small foramen of the‘‘posterolateral bridge’’ allowing a passage for the sub-occipital nerve and minor branches of the veins.

Finally, we noted that in 13 cases of CVA (72.22%) a‘‘retrotransverse foramen’’ (Fig. 9) coexisted ipsilater-ally. In cases of incomplete CVA we found the coexis-tence of an incomplete ‘‘retrotransverse foramen’’ in66.66% of the cases (Fig. 10). From the ‘‘retrotransverseforamen’’ a small vein passes through connecting theatlanto-occipital and atlanto-axoidian venous sinuses.The high incidence of coexistence of CVA and ‘‘retro-transverse foramen’’ possibly means that due to vertebralvenous plexus compression the blood flow is directedinto the small vein of the ‘‘retrotransverse foramen.’’

Discussion

In our series of atlases in which the age of the corre-sponding cadavers was known we found that theincomplete CVA appeared to be more characteristic inthe age group 5–44 years, while in an older age groupthe incomplete CVA was less characteristic. In the agegroup 45–90 years the CVA was characteristic, whichprobably means that the CVA appears after an ossifi-cation procedure has occurred in the incomplete CVA.This conclusion is supported by our finding that in66.66% of incomplete CVA, incomplete retrotransverseforamina coexisted while in 72.22% of CVA completeretrotransverse foramina coexisted, possibly meaningthat an ossification procedure occurs.

These conclusions support the findings of Taitz et al.[30] who found that an incomplete CVA was charac-teristic in the age group 10–30 years, while in those agedbetween 30 and 80 years CVA predominated. The au-thors concluded that an incomplete CVA is be the pre-cursor of a CVA. This opinion has been supported byKendrick et al. [12] who after an observation of twofemales with a unilateral incomplete CVA over a 1- to 2-year period found a unilateral radio-opaque CVAdeveloping. In contrast, the association of bridging withaging has been shown by Selby et al. [28] not to benecessarily true in all cases, as in their samples theyfound the average age of atlas bridging occurring at9 years of age. In addition, the results of the study byMitchell [20] do not support our findings that thisoccurrence increases with age, as it appeared that theCVA has a similarly low incidence at various age groupsof adulthood, i.e., 8.7% in the age group 20–39 years,10.3% in group 40–59 years, and 10% in group 60–79 years. According to Mitchell [20], the posterior atl-anto-occipital membrane at the edge of which bonyspicules form the CVA, is not subject to severe stressduring normal head and neck movements. Contrary tothis claim, we believe that injuries of the neck hyper-flexion type are very common nowadays, particularly‘‘whiplash injuries’’ occurring during traffic accidents.During these types of injuries ruptures of the longitu-dinal, flava ligaments, and posterior atlanto-occipitalmembrane may occur [19]. At the rupture sites anossification procedure or a calcification procedure may

Fig. 3 Distribution of the CVA and incomplete CVA of the atlasvertebrae according to the age groups

Table 2 Incidence of CVA and incomplete CVA according tooccupation

CVA IncompleteCVA

n % n %

Laborers (n=32) 12 37.5 16 50Nonlaborers (n=144) 6 4.16 27 18.75Total (n=176) 18 10.23 43 24.43

Table 1 Distribution of the CVA and incomplete CVA accordingto sex

Absent CVA IncompleteCVA

n % n % n %

Males (n=90) 58 64.44 10 11.11 22 24.44Females (n=86) 57 66.28 8 9.3 21 24.42Total (n=176) 115 65.34 18 10.23 43 24.43

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occur due to a deposit of calcium salts in the formedhematoma at the rupture sites. Lamberty et al. [14]suggested that because the CVA is commonly found inprimates and lower animals it may be disappearing inhumans, as indicated by its low incidence. The sameauthors, although considering this bridge as a sign ofatlas regression, found no change in the occurrence foralmost a century.

The results of the present study suggest a minimaleffect of gender on the atlas bridging, since the CVA ofthe atlas is more common in males (11.11%) than fe-males (9.3%); however, the difference is statisticallyinsignificant. This conclusion is supported by the studiesof Selby et al. [28] and Corrucini [7]. In contrast, Taitzet al. [30] found an incidence of the CVA to be 9.2% inwhite females, the corresponding incidence being 8% inwhite males. The same authors, however, found anincidence of 10.7% in black females and an incidence of16.4% in black males. Similarly, Mitchell [20] found forwhite and black females an incidence of 10.4% and forwhite and black males an incidence of 6.3% and 10%.Kendrick et al. [12] found the ‘‘posterior bridge’’ in16.9% of the studied females and in 14.6% of the males.We agree with the statement of Taitz et al. [30] thatpossibly external mechanical factors, such as the customof carrying heavy objects on the head, could play a rolein the development of anomalies of the atlas. Our find-ing of the CVA in 37.5% of the atlas vertebraebelonging to laborers of heavy work and farmers sup-ports the above theory. Similarly, Taitz et al. [30] foundin the Middle Eastern population an unusually highpercentage of atlas bridging (57%) in comparison toother studies. We therefore believe that irrespective ofgender the CVA probably is more common in individ-uals who sustain greater stress in the region of the cra-niocervical junction.

For the incomplete CVA we found that the commonform, continually occurring, was the absence of themiddle portion of the ‘‘posterior bridge,’’ with the upperend being in most cases (94.32%) in tubercle form and inthe rest of the cases (5.68%) in spine form, while in allcases the lower end was replaced by a small spine. Wealso found that the upper and lower edge of the partial‘‘posterior bridge’’ were approximately equal in sizewhile Lamberty et al. [14] found the upper end of thebridge to be larger than that of the lower. The latterauthors found some cases in which the lower edge wasreplaced by a small tubercle.

Our finding that the bilateral CVA has the lowestincidence (1.13%), the right-only type of CVA having anincidence of 2.84% and the left-only type having thehigher incidence (5.11%) in our northern Greek samplesupports the finding of Lamberty et al. [14] who foundthe bilateral type having the lowest incidence (3.3%) andthe left-only type the highest incidence (7.7%) in askeletal sample of 60 American whites. In contrast, thebilateral CVA had the highest incidence (6.2%) followedby the left-only (4.8%) and the right-only type (2.3%) inthe total South African sample. Our finding also concurswith McAlister’s [18] finding. The concurrence betweenthe data McAlister [18], Lamberty et al. [14], and ourown study suggests that there has been no change in theincidence of this anatomical variation over that periodof time. Additionally, in our opinion, the phenomenonof the higher occurrence of the left-only type than in theright-only type of CVA cannot be contributed to anexact anatomical explanation.

Fig. 4 a Tubercle form of the upper end of the incomplete CVA.b Spine form of the upper end of the incomplete CVA

Fig. 5 The incidence of the bilateral, left-only, and right-only typesof CVA of the atlas vertebrae according to age groups

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In our study of the sample of the northern Greekpopulation we found that the range of the superoinfe-rior diameter was 5.1–6.1 mm at the right side and 4.6–5.8 mm at the left, while the anteroposterior diameterwas 5.6–6.9 mm at the right side and 6.1–7.2 mm at theleft. Pyo et al. [23] in a radiographic study of Americanwhites’ skulls measured the diameter of CVA (possiblythe anteroposterior diameter) and found a mean diam-eter of 8.5 mm with a range of 6–12 mm. More notablewere the measurements by Mitchell [20] of the diametersand the cross-sectional area of the CVA. He found themean superoinferior diameter to be 5.3 and 5.1 mm atthe right and left side, respectively, while the mean an-teroposterior diameter was 6.4 and 6.6 mm at the rightand left side, respectively. Our results concur with thoseof Mitchell, i.e., the superoinferior diameter is smallerthan the anteroposterior. One should consider that inthe presence of an enormous vertebral artery the lattercould be compressed superoinferiorly as it passes fromthe CVA of the atlas. Thiel [31] in a cadaver studymeasured the mean diameter of the vertebral artery inthat region and found it to be 4.28 and 3.83 mm on theleft and right sides, respectively. Therefore duringmanipulation of the head and neck the vertebral arterymay be compressed in the CVA, especially on the leftside if one takes into account that the left CVA is smalland the left vertebral artery is large. Moreover, theCVA decreases in size at the point where the vertebralartery is accompanied by the vertebral venous plexusand the first cervical spinal nerve. It is quite remarkable

Fig. 6 Deeply excavated contralateral ‘‘groove for vertebralartery’’ in unilateral type of CVA

Table 3 Diameters of the CVA of the males, females, and total sample (mm). Values represent the range of dimension of the canals

Superoinferior, right Anteroposterior, right Superoinferior, left Anteroposterior, left

Mean Range Mean Range Mean Range Mean Range

Males (n=90) 5.5±0.4 5.1–6.1 6.3±0.8 5.7–6.9 5.4±0.3 4.6–5.8 6.6±0.2 6.1–7.1Females (n=86) 5.4±0.4 5.2–6.0 6.5±0.4 5.6–6.8 5.2±0.5 4.6–5.7 6.7±0.4 6.3–7.2Total (n=176) 5.4±0.5 5.1–6.2 6.4±0.7 5.6–6.9 6.4±0.7 4.6–5.8 6.7±0.3 6.1–7.2

Fig. 8 The ‘‘posterolateral bridge’’ with a small foramen for thepassage of suboccipital nerve and small veins

Fig. 9 Coexistence of CVA (a) and retrotransverse foramen (b)

Fig. 7 ‘‘Lateral bridge’’ of the atlas

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that Lamberty et al. [14] studied 77 case histories ofpatients in whom the CVA was present completely andincompletely. Of these, five were diagnosed as havingsymptoms of vertebrobasilar insufficiency of unknownorigin. A further eight cases had symptoms which sug-gest a possible relationship between these and thepresence of a CVA of the atlas. The previous authorssupported the view that the symptoms of vertebrobasi-lar insufficiency may be caused by the presence of theCVA around the vertebral artery in the absence ofidentifiable arterial disease, and that it may be a pre-disposing factor when arterial disease is present. It isconsidered by the same authors that in the event ofarteriosclerosis the presence of that CVA may be apredisposing cause of symptoms which might otherwisenot arise.

The high incidence of coexistence of CVA with‘‘retrotransverse foramen’’ possibly means, in ouropinion, that due to compression of the vertebral veinsin CVA the blood flow is directed into the small veinconnecting the atlanto-occipital and atlanto-axoidianvenous sinus, the so-called vein of the retrotransverseforamen. The presence of the ‘‘retrotransverse foramen’’is a phylogenetic characteristic of humans since the effectof gravity in the upright human drains blood from thecranium largely into the vertebral venous plexus [16, 21].We also believe that the deeply excavated contralateral‘‘groove of the vertebral artery’’ in most cases (93.5%)of unilateral CVA might be evidence that due to verte-bral artery compression in the canal the contralateralvertebral artery is dilated, causing an increase in thedepth of the corresponding groove. We consider that theresults of our study support the work of those authorswho believe that the existence of CVA or incompleteCVA is a predisposing factor for a vertebrobasilarinsufficiency.

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