posterolateral tunnels and ponticuli in human atlas vertebrae

5
J.Anat. (2001) 199, pp. 339–343, with 6 figures Printed in the United Kingdom 339 Short Report Posterolateral tunnels and ponticuli in human atlas vertebrae MAHDI HASAN, SANJEEV SHUKLA, M. SHAKIL SIDDIQUI AND DHANRAJ SINGH Department of Anatomy, King Georges Medical College, Lucknow U.P. India (Accepted 19 January 2001) The posterolateral tunnel on the superior surface of the first cervical (atlas) vertebra is of normal occurrence in monkeys and other lower animals, but its presence in the form of a tunnel-like canal, for the passage of the third part of the vertebral artery over the posterior arch of the human atlas vertebra is not reported. The aim of the present study was to detect the presence of such a canal, in addition to other types of ponticuli (little bridges) reported by earlier investigators, in macerated atlas vertebrae and routine cadaveric dissections. The posterolateral tunnel was detected in 114 %, and the posterior and lateral ponticuli in 657 and 2 % of vertebrae. Probably the bony roof of the posterolateral tunnel serves the purpose of additional lateral extension for the attachment of the posterior atlanto-occipital membrane in quadrupeds, where the load of the head is supported by the extensor muscles of the neck, ligaments and posterior atlanto-occipital membrane. In man, where the weight of the head is borne by the vertical loading of the superior articular process of the atlas, the roof of the tunnel has disappeared. Key words : Spine ; atlas ; erect posture. The posterior arch of first cervical vertebra (atlas) has been extensively investigated for its clinical signifi- cance in connection with the craniovertebral junction (CVJ) and for vascular lesions of the posterior cranial fossa. As 1 of 3 bony components of the CVJ, the atlas constitutes a clinically significant entity mainly be- cause of the importance of its grooves and foramina in the region of its posterior and lateral margins (first pointed out in the human atlas vertebra by Hoare, 1953). The sulcus situated on the posterolateral margin of the atlas forms a groove for the vertebral artery which varies in size and depth from merely an impression to a clear groove or sulcus for the passage of the artery. At times, the sulcus is bridged by an anomalous ossification and a posterior ponticulus ; occasionally a lateral ponticulus is formed. For the foramen of the posterior ponticulus, the terms ‘ foramen sagittale ’ and ‘ foramen atlan- toideum posterior ’ were coined by Loth-Niemirycz (1916) but were never widely used. The term Correspondence to Professor Mahdi Hasan, Department of Anatomy, King George’s Medical College, Lucknow-226 003, U.P. India. ‘ Kimmerle’s variant ’ (Kimmerle, 1930) occurs more often in the literature. Many synonyms have been used, e.g. ‘ foramen retroarticulare superior ’ (Brocher, 1955), ‘ canalis vertebralis ’ (Wolff-Heidegger, 1961), ‘ retroarticular vertebral artery ring ’ (Lamberty & Zivanovic, 1973), ‘ retroarticular canal ’ (Mitchell, 1998 a) and ‘ retrocondylar vertebral artery ring ’ (Mitchell, 1998 b). The incidence of a ponticulus posterior on the 1st cervical vertebra has been studied by many investi- gators. Notably, Kendrick & Biggs (1963) examined lateral cephalometric radiographs from 353 young caucasoid orthodontic patients (age range 6–17 y) for the presence of a ponticulus posterior on the 1st cervical vertebra. Those showing a ponticulus were divided on the basis of being bilaterally complete or incomplete. The youngest female with a ponticulus was 6 y 7 mo, the oldest 16 y 5 mo. Therefore it seemed worthwhile to make a frequency distribution study of the incidence of the ponticulus posterior and also to carry out a morphometric assessment of its various types. The main objective of the present study was to

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Page 1: Posterolateral tunnels and ponticuli in human atlas vertebrae

J.Anat. (2001) 199, pp. 339–343, with 6 figures Printed in the United Kingdom 339

Short Report

Posterolateral tunnels and ponticuli in human atlas vertebrae

MAHDI HASAN, SANJEEV SHUKLA, M. SHAKIL SIDDIQUI AND DHANRAJ SINGH

Department of Anatomy, King George’s Medical College, Lucknow U.P. India

(Accepted 19 January 2001)

The posterolateral tunnel on the superior surface of the first cervical (atlas) vertebra is of normal occurrence

in monkeys and other lower animals, but its presence in the form of a tunnel-like canal, for the passage of

the third part of the vertebral artery over the posterior arch of the human atlas vertebra is not reported. The

aim of the present study was to detect the presence of such a canal, in addition to other types of ponticuli

(little bridges) reported by earlier investigators, in macerated atlas vertebrae and routine cadaveric

dissections. The posterolateral tunnel was detected in 1±14%, and the posterior and lateral ponticuli in 6±57

and 2% of vertebrae. Probably the bony roof of the posterolateral tunnel serves the purpose of additional

lateral extension for the attachment of the posterior atlanto-occipital membrane in quadrupeds, where the

load of the head is supported by the extensor muscles of the neck, ligaments and posterior atlanto-occipital

membrane. In man, where the weight of the head is borne by the vertical loading of the superior articular

process of the atlas, the roof of the tunnel has disappeared.

Key words : Spine; atlas ; erect posture.

The posterior arch of first cervical vertebra (atlas) has

been extensively investigated for its clinical signifi-

cance in connection with the craniovertebral junction

(CVJ) and for vascular lesions of the posterior cranial

fossa. As 1 of 3 bony components of the CVJ, the atlas

constitutes a clinically significant entity mainly be-

cause of the importance of its grooves and foramina in

the region of its posterior and lateral margins (first

pointed out in the human atlas vertebra by Hoare,

1953). The sulcus situated on the posterolateral

margin of the atlas forms a groove for the vertebral

artery which varies in size and depth from merely

an impression to a clear groove or sulcus for the

passage of the artery. At times, the sulcus is bridged

by an anomalous ossification and a posterior

ponticulus ; occasionally a lateral ponticulus is

formed.

For the foramen of the posterior ponticulus, the

terms ‘foramen sagittale ’ and ‘foramen atlan-

toideum posterior ’ were coined by Loth-Niemirycz

(1916) but were never widely used. The term

Correspondence to Professor Mahdi Hasan, Department of Anatomy, King George’s Medical College, Lucknow-226 003, U.P. India.

‘Kimmerle’s variant ’ (Kimmerle, 1930) occurs more

often in the literature. Many synonyms have been

used, e.g. ‘ foramen retroarticulare superior ’ (Brocher,

1955), ‘canalis vertebralis ’ (Wolff-Heidegger, 1961),

‘ retroarticular vertebral artery ring’ (Lamberty &

Zivanovic, 1973), ‘ retroarticular canal ’ (Mitchell,

1998a) and ‘retrocondylar vertebral artery ring’

(Mitchell, 1998b).

The incidence of a ponticulus posterior on the 1st

cervical vertebra has been studied by many investi-

gators. Notably, Kendrick & Biggs (1963) examined

lateral cephalometric radiographs from 353 young

caucasoid orthodontic patients (age range 6–17 y) for

the presence of a ponticulus posterior on the 1st

cervical vertebra. Those showing a ponticulus were

divided on the basis of being bilaterally complete or

incomplete. The youngest female with a ponticulus

was 6 y 7 mo, the oldest 16 y 5 mo. Therefore it

seemed worthwhile to make a frequency distribution

study of the incidence of the ponticulus posterior and

also to carry out a morphometric assessment of its

various types.

The main objective of the present study was to

Page 2: Posterolateral tunnels and ponticuli in human atlas vertebrae

1

2

3 6

5

4

Figs 1–6. Human atlas vertebrae showing morphological features on their posterior arches : impression for vertebral artery (Fig. 1) ;

distinct groove (Fig. 2) ; partial posterior ponticulus (Fig. 3) ; complete posterior ponticulus (Fig. 4) ; lateral ponticulus (Fig. 5) ; and

posterolateral tunnel (Fig. 6). Note that in Fig. 6 a dehiscence (^) is seen on the left side.

investigate the incidence and to measure the

dimensions of the posterolateral tunnel, lateral

ponticulus and posterior ponticulus of the atlas

vertebrae in the available skeletal material.

The observations were made on 350 dried macerated

north Indian atlas vertebrae of either sex obtained

from the collections of the Department of Anatomy,

King George’s Medical College, Lucknow, India. In

addition, dissection of well preserved cadavers (30–

60 y of age) was performed to expose the 2nd and 3rd

parts of the vertebral artery and thus to determine the

incidence of ponticuli (bridges) on the posterior arch

of the atlas vertebrae. Attention was paid to features

on the superior surface of the atlas.

Measurements were taken of the maximum

dimensions of the foramina transversaria (in the

ventrodorsal and mediolateral planes) and of the

ponticuli and tunnels (in the ventrodorsal and rostro-

caudal planes).

The cross-sectional areas of the foramina, ponticuli

and tunnels were calculated from the above measure-

ments using the formula for the area of an ellipse :

Area (A)¯π¬D"¬D

#¬"

%(Mitchell, 1988a).

340 M. Hasan and others

Page 3: Posterolateral tunnels and ponticuli in human atlas vertebrae

The metric data were analysed statistically for any

significant difference using 2-way Student’s t test. P

values ! 0±05 were considered significant.

The dried vertebrae (n¯ 350) were classified on the

basis of the features on their posterior arches for the

passage of the vertebral artery from the foramen

transversarium up to the margins of the vertebral

foramen. Six classes could be identified (Figs 1–6) :

class I, where an impression for the vertebral artery

was noticeable on the posterior arch (Fig. 1) of the

vertebra, (n¯ 166) ; and class II, where the impression

for the artery was deeper than the former class. It was

seen as a distinct groove or sulcus (Fig. 2) in 150

vertebra.

In the remaining 34 vertebrae, a ponticulus or

bridge on one or both sides of the posterior arch was

a noticeable feature. These 34 vertebrae could there-

fore be further classified as one of the following: class

III, where a partial posterior ponticulus was noted as

a bony spicule (Fig. 3) extending from the superior

articular facet overhanging the dorsal arch (n¯ 11).

In some the spicule projected from the arch towards

the superior articular process ; class IV, where a

complete posterior ponticulus (Fig. 4) could be

detected (n¯ 12) ; class V, where a lateral bridge (Fig.

5) extended from the lateral mass to the transverse

process (n¯ 7) ; class VI, where a relatively more

extensive posterolateral tunnel (Fig. 6) made its

appearance as a combination of complete posterior

(class IV) and lateral (class V) bridges (n¯ 4) ; in all 4,

the posterolateral tunnels extended from their for-

amina transversaria to the medial aspect of the

superior articular facets.

Table 1 depicts the incidence of these different

classes of atlas vertebrae.

It was noteworthy that posterolateral tunnels were

found on one side only. In 2 vertebrae the tunnel was

on the left side. By contrast, the posterior and lateral

ponticuli were either present bilaterally or were seen

on one side only (Table 2).

Table 1. Distribution of atlas vertebrae on the basis of

features on dorsal arches

Class %

I 47±40

II 42±90

III 3±14

IV 3±42

V 2±00

VI 1±14

Table 2. Incidence of ponticuli and posterolateral tunnels for

vertebral artery in human atlas vertebrae (n¯ 350)

Ponticuli (groups) Bilateral

Unilateral

Right Left

Posterior (n¯ 23)

III (n¯ 11) 4 (1±14%) 3 (0±86%) 4 (1±14%)

IV (n¯ 12) 3 (0±86%) 4 (1±14%) 5 (1±42%)

V (n¯ 7) 1 (0±29%) 2 (0±57%) 4 (1±14%)

VI (n¯ 4) — 2 (0±57%) 2 (0±57%)

Table 3. Average dimensions and cross-sectional area of

foramina transversaria in human atlas vertebrae with

ponticuli (n¯ 34)

Class

Ventrodorsal

dimension (mm)

Mediolateral

dimension (mm)

Cross-sectional

area (mm#)

Right Left Right Left Right Left

IV 8±25 8±33 7±70 8±17 53±79 51±46

V 8±13 8±67 7±00 6±83 46±68 51±14

VI 7±50 9±25 7±75 8±50 52±81 50±67

Table 4. Average dimensions and cross-sectional area of

ponticuli in atlas vertebrae (n¯ 34)

Class

Ventrodorsal

dimension (mm)

Rostrocaudal

dimension (mm)

Cross-sectional area

(mm#)

Right Left Right Left Right Left

IV 8±80 8±50 7±30 7±00 46±75 50±28

V 7±25 7±50 7±00 7±00 42±85 39±88

VI 8±50 8±16 6±50 7±50 48±01 54±42

No significant change was observed in the

dimensions of the foramina transversaria in either

planes or on either side, except in class VI where the

ventrodorsal dimension was significantly larger on

the left than on the right (Table 3). The cross-sectional

area of the class V vertebrae was also significantly

smaller on the right.

The cross-sectional areas of the different types of

ponticuli and posterolateral tunnels are given in Table

4. Comparing this table with Table 3 shows that the

cross-sectional areas of the ponticuli are in general

smaller than the foramina transversaria.

Although varying incidences of posterior and lateral

ponticuli (bridges) have been reported (Table 5), we

have found no mention of a tunnel-like bony canal on

the posterior arch of human vertebrae in the literature.

Posterolateal tunnels and ponticuli in human atlas vertebrae 341

Page 4: Posterolateral tunnels and ponticuli in human atlas vertebrae

Table 5. Comparison of the reported incidence of ponticuli in

human atlas vertebrae with the present findings

Study

Incidence of ponticuli (%)

Posterior Lateral

Poirier (1911) 8±00 —

Le Double (1912) 11±70 1±80

Loth-Niemirycz (1916) 7±40 —

Barge (1918) — 2±30

Dubreuil-Chamberdel (1921) 30±00 —

Hayek (1927) 10±00 2±90

To$ ro$ & Szept (1942) 18±00 3±50

Radojevic & Negovanovic (1963) — 2±50

Lamberty & Zivanovic (1973) 15±00 —

Malhotra et al. (1979) 5±14 0±80

Taitz & Nathan (1986) 7±80 —

Dhall et al. (1993) 37±83 13±50

Prescher (1997) 11±00 —

Mitchell (1998a, b) 9±80 12±24

Present study* 6±57 2±00

* We detected posterolateral tunnels in 4 of 350 (1±14%) atlas

vertebrae in addition to the ponticuli. None of the above workers

mentioned anything about such tunnels in human atlas vertebrae,

except Prescher (1997) who reported a 1±5% incidence of

posterolateral ponticuli.

We found a posterolateral periarticular bony tunnel

on the superior surface of 4 of 350 atlas vertebrae.

Several factors responsible for the posterior and

lateral bridging of atlas vertebrae have been proposed,

but the appearance of the bony tunnel observed by us

indicates a reduction in the cross-sectional areas of the

ponticuli and tunnels compared with that of the

foramina transversaria. This cannot be accounted for

by any of the explanations so far proposed.

The origin of the bridges is a matter of much

debate. Allen (1879), Cleland (1960) and von To$ rklus

& Gehle (1975) suggested that it was a congenital

characteristic ; Selby et al. (1955) suggested that it was

a genetic trait ; while others (Pyo & Lowman, 1959;

Epstein, 1955; Breathnach, 1965; White & Panjabi,

1978) said that it could be the result of ossification due

to ageing. The findings of Taitz & Nathan (1986) lend

credence to the latter theory, in American white and

Negro population groups. These authors considered

that a study on Bedouin women would be of interest

to determine whether external mechanical factors,

such as the custom of carrying heavy objects on the

head, could play a role in the development of bridges

on the atlas.

Breathnach (1965) associated the ossification of the

oblique ligament of the atlas with the ponticulus

posterior. Prescher (1997) discounted the theory that

the ponticulus posterior represents an acquired ossi-

fication of ligaments induced by the pulsation of the

vertebral artery (Le Double, 1912) or an activation of

existing special osteogenetic potency in the region of

the craniovertebral junction (Barge, 1918), since

cartilaginous ponticuli posterior have been observed

in fetuses and children (Lamberty & Zivanovic, 1973).

When dissecting the cadavers, we noticed that the

oblique ligament of the atlas is not an independent

structure but the lower border of posterior atlanto-

occipital membrane. This corroborates the findings of

Lamberty & Zivanovic (1973).

Interestingly, Mitchell (1998a) credits Lamberty &

Zivanovic (1973) with the statement that the lateral

bridge and retroarticular canal are not only common

in lower vertebrates but also occur in primates. But

in their own report, Lamberty & Zivanovic (1973)

maintained that a bony ring for the vertebral artery is

a common structure in other vertebrates, and le

Double (1912) gave an extensive description of the

ring in primates and other vertebrates. Lamberty &

Zivanovic (1973) themselves did not study atlas

bridging in primates and other vertebrates. Mitchell

(1998a) has given a new classification of atlas

vertebrae based on the degree of formation of

retroarticular canals for the passage of the vertebral

artery. Those atlas vertebrae with a complete bony

ring over their posterior arch have been described as

‘class III ’ both by Taitz & Nathan (1986) and Mitchell

(1998a). In support of this classification, our study

detected posterolateral tunnels (Class VI) on the

superior surface of 4 atlas vertebrae. This class of

vertebrae represents the posterolateral tunnel found in

primates, which seems to be the most primitive feature

of the human atlas vertebra. Furthermore, we have

noted a dehiscence of the inferior part of the middle of

theposterolateral ponticulus in 4of 350atlas vertebrae.

It is apparent that an extension of this gap rostrally

would cause the separation of the lateral and posterior

ponticuli. The lateral ponticuli, whose incidence is

much lower (2%), may be lost early in development,

with the result that the posterior ponticuli persist in

larger number of instances (6±57%). It is noteworthy

that the posterior bridging regresses by the dis-

appearance of its middle part first, thus explaining the

occurrence of partial bridging (Class III). However, in

the great majority of cases, either a sulcus for the

vertebral vein and artery (42±9%), or simply an

impression for these vessels (47±4%), is detected.

The bony roof of the posterolateral tunnel probably

allows greater lateral attachment of the posterior

atlanto-occipital membrane in quadrupeds where the

load of the head is supported by the extensor muscles

of the neck, ligaments and the posterior atlanto-

occipital membrane; but in man—where the weight of

head is borne by vertical loading of the superior

342 M. Hasan and others

Page 5: Posterolateral tunnels and ponticuli in human atlas vertebrae

articular process of atlas—the roof of tunnel has

disappeared.

The posterior and lateral bridging and postero-

lateral tunnels were more commonly observed on the

left side. Dhall et al. (1993) observed an increased

incidence of bridges on the left, correlated with the

larger superior articular facet on that side. They

hypothesised that this asymmetry in the occurrence of

bridges may be due in part to unequal weight-bearing

as a result of more commonly left-tilted head posture.

Owing to the right-sided dominance of muscles of the

body in right-handers, the larger and consequently

stronger right sternocleidomastoid would tend to tilt

the head to the opposite side (Pande & Singh 1971). It

is apparent that the posterior and}or lateral bridging,

and the posterolateral bony tunnel, would in extreme

cases further compromise the calibre of an already

stretched vertebral artery. Ercegovac & Davidovic

(1970) alleviated the symptoms of vertebrobasilar

insufficiency by surgical removal of the bony ring in 8

cases.

The cross-sectional areas of the ponticuli have been

found to be smaller than the areas of foramina

transversaria. Based on these considerations, the

posterolateral ponticuli might predispose to a per-

ipheral compression syndrome. Clinical investi-

gations, particularly where the 3 manifestations of the

ponticuli are differentiated precisely, as yet do not

exist.

We thank the Indian Council of Medical Research for

the financial assistance for this project (E.M.S to

M.H, and R.A. to S.S.). The authors are grateful to

Professor Ashok Sahai, head of the Department of

Anatomy, for his invaluable research facilities, and to

Dr Anita Rani and Professor G. N. Verma for cross-

checking the measurements.

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Posterolateal tunnels and ponticuli in human atlas vertebrae 343