CT of the main ligaments of the cervico-occipital hinge J.-L. Burguet 1, H. Sick 2, Y. Dirheimer 1, and A. Wackenheim 1 1Department o f Radiology and 2Anatomical Institute, University Louis Pasteur, Strasbourg, France
Summary. The results of a CT-anatomical correlative study of the main ligaments of the cervico-occipital hinge are reported. CT criteria of normal ligamentous structure of this region are presented in axial, coronal and sagittal views with a special attention to the transverse ligament of the Atlas. Examples of pathological transverse ligaments are illustrated and emphasis is laid upon the better statement CT allows in such cases. Key words: Transverse ligament - alar ligaments -
More than half a century elapsed since the Anatomical School in Strasbourg started to pay a special attention to the cervico-occipital hinge. First in 1922 P.Hecker published his comparative anatomical study of the cervico-occipital ligamentous system ; more recently, and before CT developments, one of us devoted a monograph to this major functional region . We want to continue this work by enlarging the contribution of CT. In this first paper we intend to demonstrate the normal transverse and alar ligaments; we shall end by presenting a few pathological examples.
ted to the same CT procedure using a CE 10,000 total body scanner (CGR). We attempted the most precise positionning of items for axial, sagittal then coronal sections by testing the symmetry of their osseous structures around the midline both on preliminary scout-views and on the first CT slices obtained. The refering scanning planes were as follows: - Axial section: plane passing through C 1 and parallel to the plane of Frankfort and/or plane passing through the anterior and posterior arches of the atlas vertebra (plane of C1); - Sagittal section: slices parallel to the sagittal plane and extending from the midline to the lateral articular process of C 1 ; - Coronal section: slices parallel to the coronal plane o f the dens of C2 and extending from the top of the dens to the anterior aspect of the medulla. The examination was then carded out using the following parameters: slice thickness: 1 mm, scaning time: 6.8 seconds with 130kV and 80mA, and systematic reformatting with a high spatial resolution computed program (512 x 512 matrix). Table t. See text Densities
( + 15 HU):
Post m o ~ e m
Material and method
A CT-anatomical correlative study was performed using five anatomical specimens consisting of detached heads of adults. All specimens were submit-
72 72 78 75 76 110 103 92 98
Sagittal plane 50 47 66 8 5
55 60 40 50 78 -
108 105 101 110
Sagittal plane 35 -
Fig.la-e. Axial CT slice a and histologic anatomical view b through the transverse ligament of the atlas (plane of Frankfort): 1: Pharyngeal cavity, 2: Stylo'id process, 3: Mastoid process, 4: Odontoid process, 5: Transverse ligament, 6: Lateral mass of C 1, 7: Alar ligament, 8: Anterior epidural venous plexus, 9: Membrana tectoria, 10: Fatty cellular plane, 11: Dura mater, 12: Spinal cord. c Histological view of the midportion of the transverse ligament: the transverse ligament is formed from dense bundles of collagen within its posterior portion (1). Its anterior midportion (2) is infiltrated with chondroid cells and is tightly applied on the posterior aspect of the dens which is covered with fibro-cartilaginous tissue (3). d Histological view of the right lateral portion of the transverse ligament: several bundles (1) infiltrated with lax connective tissue (2) are fanning out and anchor themselves on the tubercles of the lateral mass of C 1 (3). Synovial fringes (4) are visible within the lateral part of the articular interspace, e Using a wide window setting the tubercles of the lateral masses of C 1 are perfectly seen (white arrows). Their normal inner edge is covered with thick and regular cortical bone. Note the sharp retro-tubercular groove on the right side
M a t e r i a l w i t h d e g e n e r a t i v e o s s e o u s c h a n g e s at C 0-C 1-C 2 levels w a s n o t c o n s i d e r e d as n o r m a l a n d w a s e x c l u d e d f r o m this study. T h e r e m a i n i n g specim e n s w e r e f r o z e n in o r d e r to o b t a i n a n a t o m i c slices along previously marked planes consisting of scalpel i n c i s i o n s m a d e o n t h e s p e c i m e n s at t h e t i m e o f C T e x a m i n a t i o n a n d c o r r e s p o n d i n g to t h e C T levels. A n a t o m i c slices w e r e f i n a l l y p r e p a r e d f o r histological examination using hematoxylin - eosine stains.
Fig.2. Coronal CT slice of the cervico-occipitaljoints:/:Occipital bone, 2: Lateral mass of C 1, 3: Dens of axis, 4: Alar ligament
The criteria of normality of the transverse ligament o f t h e atlas a r e to b e c o n s i d e r e d b o t h o n a x i a l a n d s a g i t t a l C T s c a n s ( c o r o n a l sections, in o u r e x p e r i -
Fig. 3 a-e. Sagittal CT view a and corresponding macroscopic anatomical view b of the cervico-occipital hinge: 1: Occipital bone, 2: Anterior arch of C 1, 3: Posterior arch of C 1, 4: Dens of axis, 5: Body of C 2, 6: Apical ligament of dens, 7: Transverse ligament, 8: Cellular plane, 9: Superior longitudinal band of the cruciform ligament, 10: Dura mater, 11: Medulla oblongata, 12: Spinal cord, 13: Anterior atlanto-occipital membrane, 14: Posterior atlanto-occipital membrane, c Sagittal microscopic view of the midportion of the transverse ligament: Legend Id. a and b
Fig.4a and b. Sagittal CT view a passing through the lateral portion of the transverse ligament and corresponding histological view b: 1: Occipital bone, 2: Anterior arch of C 1, 3: Posterior arch of C 1, 4: Odontoid process, 5: Transverse ligament, 6: AIar ligament, 7: Membrana tectoria, 8: Dura mater, 9: Intra-spinal venous plexus, 10: Extra-spinal venous plexus, 11: Median atlanto-axial joint with synovial fringe
ence, do not explore the transverse ligament properly). The following are to be examined: the shape of the transverse ligament, its dimensions (essentially its thickness, normal value: 2 mm + 1 mm), its density both for its middle and its outer parts, the densities of the planes near the ligament and last of all, the osseous tubercles of C 1 which are the points of insertion of the transverse ligament. E Eckert described the transverse ligament as the transverse and main part of the ligamentum cruciformis atlantis, 2 to 3 mm thick at its medial part, separated from the posterior plane of the membrana
tectoria by fatty cellular tissue and from the posterior aspect of the dens by the cavity of the syndesmoaxoidal joint between the anterior facet of the transverse ligament and the posterior facet of the odontoid process. All these points are quite well recognizable in CT.
The transverse ligament is the main and strongest ligament of the cervico-occipital hinge. It is also the most visible ligament of the cervico-occipital region
Fig.5. Rheumatoid arthritis: the transverse ligament is mainly calcified within its medial and left parts, as well as within its insertions on both sides (white arrows). The anterior atlanto-axial joint is filled with an isodense mass of inflammatory tissue which produces a diastasis between C 1 and C 2. The syndesmo-axoi'dal joint is visible behind the dens but is too wide and isodense, so that it may be said that this joint is probably affected too by the inflammatory desease
in axial CT, both parallel to the plane of Frankfort and through the plane of C 1. Typically the transverse ligament appears as a thick and regular stripe, concave forward around the posterior aspect of the dens (Fig. 1 a). This stripe stands out with its marked hyperdensity, higher in the midline, just behind the dens, than at the level of the insertions of the transverse ligament on each side. Indeed the mean density value of the transverse ligament in anatomy specimens reaches 74 HU for its medial part, and 56 HU for its outer parts. In vivo the density values are even higher (Table 1). This difference in density values between the medial and the lateral parts of the transverse ligament is well correlated to its histological structure. Layers of collagen are thicker and more closely paded in the central portion of the ligament than laterally where the fibrous sheaves fan out to reach the tubercles of the atlas (Fig. 1 a, b, c and d). The hyperdense stripe representing the transverse ligament on CT is all the more visible as it is separated from adjacent structures by hypodense aeras. Very distinctive indeed are the planes of different densities on each side of the ligament. These are, from back to front: the dura-mater spontaneously hyperdense, indistinguishable from the membrana tectoria, concave backward; then the fatty sliding
Fig. 6. Rheumatoid arthritis: the left portion of the transverse ligament is no longer visible and is replaced by a hypodense area (white arrows). This area is in relation with the huge hypo-isodense zone developed within the anterior atlanto-axial joint and corresponding to the inflammatory pannus. In such a case the diastasis is due both to the involvement of the anterior atlanto-axial joint and to the destruction of the transverse ligament
Fig. 7. Left hemi-occipitalisation of the atlas vertebra: In this case, aplasia of the transverse ligament does not accompany the bony malformation. CT demonstrates quite well the presence of the transverse ligament (white arrows)
cellular plane, hypodense; then the transverse ligament proper, hyperdense; then the hypodense articular cavity of the posterior atlanto-axial joint, extending on each side along the postero-lateral aspect of the dens; then at last, the posterior edge of the dens with its osseous density (Fig. 1 a).
Fig.8. Retrodental pyogenic abcess (white arrows) bulging into the anterior aspect of the dural sac. No transverse ligament is seen. The anterior atlanto-axial joint is extremely narrowed and the dens distorted. The left tubercle of C 1 is no longer visible (compare with the opposite side, black arrow)
its top may sometimes present a small non pathological regular cortical defect; sometimes, too, the tubercle may look more or less quadrangular. All these are normal features. The retro-tubercular groove is also quite well seen, sometimes very sharp. A peculiar triangular space is formed between the lateral tubercle of C 1 and the lateral part of the transverse ligament anteriorly, the dura-mater posteriorly and the internal edge of the lateral mass of C 1 laterally; this space is normally hypodense and filled with fatty tissue and veins. Finally on the axial view, the alar ligaments may be partially and segmentally analyzed as they appear on each side of the dens as two little round hyperdense areas surrounded by hypodense soft tissue (Fig.1 a).
Coronal section This plane does not well image the transverse ligament, but the coronal section is required to show the alar ligaments in their entirety (Fig.2). In it these strong and essential ligaments look like two little quadrangular hyperdense areas lying obliquely upward and outward between the antero-lateral edges of the foramen magnum and the lateral edges of the dens. The ligaments form an obtuse angle which may reach 180 ° in man . Their density is lower than the density of the transverse ligament, around 40-50 HU. They are surrounded outlined by veins and fatty tissue. We did not succeed in demonstrating the apical ligament of the dens in this plane.
Fig.9. Acromegaly: Remarkably hypertrophied and completely ossified transverse ligament of the atlas vertebra. Mobility of the head was normal
These different planes of densities are to be considered as criteria for the normal transverse ligament and the normal posterior atlanto-axial joint. The tubercles of the lateral masses of C 1, which are the points of attachment of the transverse ligament, are of particular interest (Fig. 1 e). They have, of course, to be examined using a wide bone window. Their development is of variable importance, sometimes prominent, never absent. Their osseous internal edge is always smooth and regular; however
Sagittal CT sections are not feasible in vivo. Nevertheless this study of anatomical specimens makes the data collected in axial views more understandable. On a strictly medial slice the ligamentum cruciformis atlantis appears as an hyperdense stripe parallel to the posterior aspect of the dens of the axis (Fig. 3 a, b and c). Typically this stripe has an S-shape and always fits the posterior contour of the dens. (This explains why in older patients, the transverse ligament sometimes has a circumflex shape concave forward behind a dens the posterior edge of which is altered by arthrosis; in such a case the transverse ligament may appear thicker in axial views.) On this sagittal slice, the upper and lower parts of the hyperdense stripe may not correlate with the transverse ligament itself. Indeed our anatomical and histological studies revealed a transverse ligament, the height of which was inferior to that of the hyperdense stripe seen in CT. In fact, on a strictly
Note that on the precisely medial slice the apical ligament of the dens is well seen as a slightly hyperdense linear structure, between the anterior edge of the foramen magnum and the top of the dens (Fig. 3 a, n° 6). On more lateral sagittal CT slices, the transverse ligament rises slightly laterally to reach the corresponding tubercles of the atlas vertebra. In so doing, the transverse ligament fans out so that the shape of its section changes. The result in sagittal CT is that the lateral portion of the transverse ligament has a comma shape oblique forward and downward which has to be looked for higher than the medial part of the ligament (Fig. 4 a and b). Note finally, the anterior and posterior atlantooccipital membranes as regular hyperdense linear stripes, as well as the numerous veins surrounding the ligaments of the cervico-occipital hinge. Fig.10. Morquio's syndrome: a huge mass of tissue (1) is replacing the normal osseous dens of C 2. No transverse ligament is seen behind this mass. Anterior arch of C 1 (2); Occipital bone (3); spinal cord outlined by contrast-media (4)
Pathological examples Precise knowledge of the normal features of the main ligaments of the cervico-occipital hinge allows us to best analyze their changes under pathological circumstances, both in rheumatic diseases and other pathological entities. Rheumatoid arthritk¢
Fig. 11. Chondrocalcinosis: double curved rail aspect of the calcifications of the transverse ligament. Note that the calcification does not exactly reach the tubercle of the lateral mass of C 1. No clinical symptoms
sagittal CT slicethe upper and lower parts of the hyperdense stripe corresponded to the superior and inferior longitudinal bands of the ligamentum cruciformis, so that the height of the transverse ligament could not be precisely measured here. As in axial CT sections, the different planes of densities on each side of the transverse ligament are still easily recognizable (Fig. 3 a).
Involvement of the cranio-cervical region in rheumatoid arthritis is well known and has been systematically investigated. Castor et al.  have recently explored this pathology by CT. We present here two different cases of altered transverse ligaments in rheumatoid arthritis. The first (Fig. 5) was a 60-year-old woman in whom the transverse ligament appeared almost completely calcified. The articular cavity of the posterior atlanto-axial joint was still clearly seen. Diastasis was seen between the anterior arch of C 1 and the dens all this region being filled with hypo- and isodense inflammatory tissue. The second case was a 65-year-old woman presenting with involvement of her pyramidal tract. The left part of the hyperdense normal transverse ligament was replaced by relatively hypodense tissue. The dens was irregular in shape and the anterior C 1-C 2 joint was enlarged and filled with isodense inflammatory tissue (Fig. 6). In such cases CT allows a better appreciation of involvement of the different soft structures of the cervico-occipital region as well as a better control of the evolution of the lesions under treatment.
Malformative pathology Fig. 7 is a case of occipitalisation of the atlas vertebra in a young child. CT demonstrates in this case the existence of a transverse ligament although there was a slight lateral subluxation of the dens. CT has some prognostic value in this case.
Infections Osteitis of the dens is rare and more often seen in debilitated patients. The case presented here (Fig. 8) was a 54 year old man suffering from infected lung carcinoma and quadriparesis. CT showed the altered and irregular edges of the dens, as well as the presence of a huge hypodense mass bulging onto the anterior aspect of the dural sac. The transverse ligament was no longer visible. Surgery revealed a pyogenic abcess and complete destruction of the transverse ligament.
Miscellaneous Acromegaly constantly involves the spine. The illustration, Fig. 9 is of a 41-year-old man where the transverse ligament was completely ossified and of remarkably increased thickness, slightly impressing the anterior aspect of the dural sac. No clinical symptoms were present in relation to this anomaly. Morquio's syndrome probably always involves the cervico-occipital hinge. S.J.Lipson  reported the possibility of an hypertrophied posterior longitudinal ligament. We had the opportunity to perform a CT scan in a 13 year old boy suffering from Morquio's syndrome with quadriparesis (Fig. 10). In this case the odontoid process was absent and replaced by an isodense mass of fibrous tissue, bulging backward onto the medulla. No transverse ligament was seen. Chondrocalcinosis may be defined as the presence of calcium-containing salts within articular fibro- and hyaline cartilage . In this way, the syndesmo-axoidal joint between the posterior aspect of the odontoid process and the anterior aspect of the transverse ligament may be involved. In such cases CT may reveal a peculiar picture of the transverse ligament: this one indeed presents a double hyperdense calcium deposit within its medial and lateral parts forming the image of a double regular curved rail; the inner part of this rail, close to the dens is thin and spotted, whereas its outer part is more thick and dense (Fig.ll). This calcification does not exactly reach the tubercles of the lateral masses of C 1 which are normal. No other anomaly of the soft tissues near the transverse ligament was noted: however, the alar
ligaments may sometimes be involved and appear then as two highly hyperdense calcified round areas on each side of the dens.
Conclusion Only CT can directly explore the ligamentous tracts of the cervico-occipital hinge. The high information content of millimetric CT slices with improved spatial resolution must picturing first the normal configuration of these structures, then their pathological changes, allow a better diagnostic understanding and even a better therapeutic approach to the lesions of this major functional region.
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Received: 12 April 1984
Professeur A. Wackenheim Service de Radiologie I Pavilion Clovis Vincent CHR de Strasbourg BP 426 F-67091 Strasbourg Cedex France