Posterolateral tunnels and ponticuli in human atlas vertebrae

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1 J.Anat. (2001) 199, pp , 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) ABSTRACT 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. INTRODUCTION The posterior arch of first cervical vertebra (atlas) has been extensively investigated for its clinical significance 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 because 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 atlantoideum posterior were coined by Loth-Niemirycz (1916) but were never widely used. The term 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 investigators. 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 Correspondence to Professor Mahdi Hasan, Department of Anatomy, King George s Medical College, Lucknow , U.P. India.

2 340 M. Hasan and others 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. MATERIAL AND METHODS 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 rostrocaudal planes). The cross-sectional areas of the foramina, ponticuli and tunnels were calculated from the above measurements using the formula for the area of an ellipse: Area (A) π D D (Mitchell, 1988a).

3 Posterolateal tunnels and ponticuli in human atlas vertebrae 341 The metric data were analysed statistically for any significant difference using 2-way Student s t test. P values 0 05 were considered significant. Table 2. Incidence of ponticuli and posterolateral tunnels for vertebral artery in human atlas vertebrae (n 350) Unilateral RESULTS Ponticuli (groups) Bilateral Right Left 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 therefore 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 foramina 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 % 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 Mediolateral Cross-sectional area (mm ) Right Left Right Left Right Left IV V VI Table 4. Average dimensions and cross-sectional area of ponticuli in atlas vertebrae (n 34) Class Ventrodorsal Rostrocaudal Cross-sectional area (mm ) Right Left Right Left Right Left IV V VI 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. I II III IV V VI DISCUSSION 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.

4 342 M. Hasan and others 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) Loth-Niemirycz (1916) 7 40 Barge (1918) 2 30 Dubreuil-Chamberdel (1921) Hayek (1927) To ro & Szept (1942) Radojevic & Negovanovic (1963) 2 50 Lamberty & Zivanovic (1973) Malhotra et al. (1979) Taitz & Nathan (1986) 7 80 Dhall et al. (1993) Prescher (1997) Mitchell (1998a, b) Present study* * 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 ossification 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 atlantooccipital membrane. This corroborates the findings of Lamberty & Zivanovic (1973). Interestingly, Mitchell (1998 a) 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 (1998 a) 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 (1998 a). 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 the posterolateral ponticulus in 4 of 350 atlas 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 disappearance 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 atlantooccipital membrane; but in man where the weight of head is borne by vertical loading of the superior

5 Posterolateal tunnels and ponticuli in human atlas vertebrae 343 articular process of atlas the roof of tunnel has disappeared. The posterior and lateral bridging and posterolateral 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 peripheral compression syndrome. Clinical investigations, particularly where the 3 manifestations of the ponticuli are differentiated precisely, as yet do not exist. ACKNOWLEDGEMENTS 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 crosschecking the measurements. REFERENCES ALLEN W (1879) On the varieties of the atlas in the human subject and the homologies of its transverse process. 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