The Neuroradiology Journal 20: 209-217, 2007
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Biomechanics of the Spine III. The Cranio-Cervical Junction R. IZZO, G. AMBROSANIO, A. CIGLIANO*, D. CASCONE**, G. GALLO***, M. MUTO Neuroradiology Department A.O.R.N., A. Cardarelli; Napoli, Italy * Emergency Neurosurgery Department A.O.R.N., A. Cardarelli; Napoli, Italy ** Graduate in Medicine, external collaborator *** CDS Portici; Napoli, Italy
Key words: biomechanics, cranial-cervical junction, traumas, spinal instability
SUMMARY – By virtue of its unique anatomy and functions the cranial-cervical junction was excluded in previous reviews on the general biomechanics of the spine, being a world apart. The special design of the cranial-cervical (CCJ) junction responds to seemingly opposed necessities being at same time loose enough to allow a great variety of movements and strong enough to preserve the spinal cord and vertebral arteries and to resist the head weight and muscular action. The primary goal of the CCJ is to ensure the maximal mobility of the head for visual and auditory exploration of space. Like a cardan joint the CCJ allows simultaneous independent movements about three axes in order to repeat and extend eye movements under the control of vestibular receptors. Several muscular groups and a number of ligaments control the movements of the CCJ and ensure its stability. Although composed of two seemingly distinct joints the CCJ forms a unique functional complex whose stability is ensured by ligaments and bony restraints often operating on both joint components: the occipitoatlantal and atlantoaxial joints.
Introduction The Functional Program of the CCJ
The cranial-cervical junction (CCJ) is a transitional structure programmed to ensure maximum mobility of the head for the visual and auditory exploration of space (figure 1). In order to obtain a stereoscopic vision and the fusion of the images coming from both halves of the visual scene the light pulses have to be direct on the maculas which having the highest concentration of cones account for the maximal visual resolution and for as much as 8/10° of visual acuity. For this purpose the co-ordinated action of the orbital muscles performs fine adjustments in a range of about 30° in both horizontal and vertical planes over which the precision of movements fades. A complete exploration of space demands coupled movements of the eyeballs and the head. The co-ordinated activity of the eyes and
the head is a very complex program mainly relying on: – a special fibre tracts association referred to as the medial longitudinal fasciculus (MLF) directly and indirectly, through the reticular formation, connecting the vestibular nuclei, in turn stimulated by the gravity and acceleration receptors of the labyrinths, and extraocular muscles and XI nerve nuclei controlling the eyes, head and neck movements, respectively 1,20,21 . – a special mechanical device: the CCJ allowing the head to perform and extend the same movements as the gaze. All four vestibular nuclei send direct and crossed outputs on III, IV e VI nerve nuclei via ascending components of the MLF with inhibitory and excitatory effects respectively, controlling the conjugate eye movements 1. Like a cardan system, the CCJ realizes two separate degrees of freedom with simultaneous and independent movements about three axes 20,21: 1. flexion-extension around a transversal axis; 209
Biomechanics of the Spine III. The Cranio-Cervical Junction
2. axial rotation around a vertical axis; 3. instantaneous, from the combination of 1 and 2. The one and two axes are fixed, the third is variable. Thanks to the CCJ the neck muscles can perform a great variety of movements at same time attaining a precise control of any single movement. By virtue of its special anatomy the C0-C1-C2 complex allows high freedom of movements being strong enough to preserve the spinal cord and vertebral arteries and to support the head weight and muscle action. Kinematics of the CCJ The occiput-C1-C2 complex as a whole accounts for 40% of all cervical flexion-extension and 60% of global rotation. The average movements performed by two components of the CCJ are summarized in table 1 17,19. Table 1 Movements of the CCJ
Joint
Motion
Range of Motion
C0-C1
flexion-extension lateral bending (unilat.) axial rotation (unilat.)
25° 05° 05°
C1-C2
flexion-extension lateral bending (unilat.) axial rotation (unilat)
15° 05° 40°
The occipitoatlantal joint This joint consists of spherical articulations cobered by tough capsules which contribute to joint stability. The primary movement of the occiput-C1 joint is flexion-extension during which the occipital condyles rotate and move in posterior and anterior directions, respectively 5 (figure 2). Table 2 indicates the elements restraining these movements: Restrainers of Flexion
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During flexion-extension the tectorial membrane and alar ligaments prevent sagittal translation between the basion and the tip of the dens whose range must not exceed 1 mm 23,25 , with a minor stabilising contribution coming from the cup-like facets of C1 (figure 3). About 5° of both axial rotation and lateral bending are also allowed 10,17, both checked by the alar ligaments 7, while axial rotation is also limited by the superior facets of C1 (figure 4). The atlantoaxial joint The C1-C2 joint, the most mobile individual joint of the cervical spine, performs most of the head’s rotation, with the atlas ring pivoting about the dens while the lateral masses slide upon the facets of C2 in opposite directions, favoured by the convexity of the surfaces limiting the reciprocal contact, and by loose capsules (figure 5). Because of the convexity of the articular surfaces C1 descends in relation to the superior facets of C2 during axial rotation. In the subaxial cervical spine the inclination of the facets allows much less axial rotation. Panjabi et Al 18 reported a general tendency to decrease with aging for all movements of the cervical spine, except the axial rotation of the CCJ. According to Rabichong 20,21 axial rotation is performed by two muscular systems: – a profound group composed of the superior and inferior obliqui muscles (SOM) (IOM); – a superficial group with the sternocleidomastoid (SCM), splenius capitis (SCA) and splenius cervicis (SCE) muscles. The IOM performs the first 30°of head rotation with a relatively fine action through its insertions on the transverse process of C1 and the spinous process of C2 (figure 6). This traction, unilateral and not balanced, creates a backwards translation of the atlas ring blocked by the contact with the dens. The movement is therefore continued by the opposed actions of the SCM and SCA whose superior insertions are located laterally on the Restrainers of Extension
Basion-tip of the dens contact
Tectorial membrane tension
posterior atlantooccipital membrane tension capsular tension alar ligaments tension posterior muscles tension oral floor-neck contact
anterior atlantooccipital membrane tension capsular tension occiput-dorsal arc of C1 contact suboccipital muscles compression
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The Neuroradiology Journal 20: 209-217, 2007
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Figure 2 A-C A) During extension of the head the occipital condyles rotate and slide forwards in the cup-shaped superior facets of C1. The opposite movements occur during the flexion (C). The sliding movements are stressed by the varying positions of the red asterisks used as reference points.
Figure 1 Diagram of a coronal section of both C0-C1 and C1-C2 joints. AO: occipitoatlantal joint. AAL: lateral atlantoaxial joint.
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Figure 4 The C0-C1 joint also performs a limited axial rotation, restrained by the cup-shaped facets of C1 in which the occipital condyles have to rise for displacement. From Diano, with permission 5.
Figure 3 Lateral view of the C0-C1-C2 joints. The normal distance between the tip of the dens and the basion is 4 to 5 mm (A). Any change in this gap over 1 mm during the flexionextension of the head with a normal transverse ligament indicates instability of C0-C1 joint. Also important for evaluation are the distances between the dens and the anterior ring of C1 (B) and the anterior cortex of the posterior C1 ring (C).
Figure 5 During the axial rotation of the head the C1-C2 lateral joints slide easy in opposite directions favoured by the convex surfaces reducing the reciprocal contact. At the end of the movement the lateral masses of C1 slightly descend in relation to the superior facets of C2 (vertical arrow). From Diano, with permission 5.
mastoids, while the inferior attachments are near the median line in order to obtain the maximal rotation possible in spite of a twitch capacity of just one-third of muscular length (figure 6) 20,21. The SCM and SCA have a powerful balanced
action. Their oblique orientation creates simultaneous compressive forces having a stabilising role, but also being responsible for mechanical stress and degenerative modifications 20 on the joints below. The alar ligaments’ tension limits the axial rotation 23 (figure 7). 211
Biomechanics of the Spine III. The Cranio-Cervical Junction
R. Izzo
The C1-C2 junction also allows about 15° of flexion-extension restricted by the tectorial membrane and the contact between bony components 17. Stability of the CCJ
Figure 6 The obliquus capitis inferior muscle (IO) performs the first 30°of head rotation via its insertions on the transverse process of C1 and the spinous process of C2. The movement is therefore continued by the opposed actions of the sternocleidomastoid (SCM) and splenius capitis (SCA) muscles located in superficial position. SCE: splenius cervicis muscle.
Figure 7 A-C Diagram of the alar ligaments viewed from above. The alar ligaments are most important in controlling the range of atlas rotation. In neutral position the ligaments are lax. The tension first involves the ligament of the same side of rotation (B), then the contralateral one (C). Their intrinsic strength is very high if compared to loads they must resist. From Clark, modified 4.
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By virtue of its peculiar anatomic and biomechanical features the CCJ has specific patterns of stability completely different from the rest of the spine. Its great mobility demands a number of ligaments to control the movements and ensure stability (figure 8). An important principle in evaluating the stability of the CCJ is that, as discussed for normal movements, many ligaments and bony restraints control and stabilise not just one, but both the C0-C1 and C1-C2 compartments at the same time. In the C0-C1 joint, for example, the work of the intrinsic ligaments, the capsules and the anterior and posterior atlantoocciptal membranes, is flanked by “extrinsic” ligaments connecting the occiput and C2 12: the tectorial membrane, the alar and apical ligaments. The normal distance between the tip of the dens and the basion must be not exceed 45 mm and must never vary more than 1 mm during flexion-extension (figure 3). The most important ligaments ensuring the stability of C1-C2 joint are: - the transverse ligament; - the alar ligaments; - the apical ligament. The transverse ligament, the most important component of the cruciate ligament, avoids the anterior displacement of the atlas during axial rotation guaranteeing the free pivoting of the dens. By virtue of a special lattice arrangement of the collagen fibres the transverse ligament is most resistant to tension, with a failure strength in biomechanical tests ranging from 170 up to 700 N corresponding to about 17 to 70 kg, respectively 8. Any increase over 3 mm of the atlantodental space or reduction below 13 mm of the distance between the posterior surface of the dens and anterior cortical of the posterior ring of C1 can occur only in case of failure of the transverse ligament (with an intact dens) whose action cannot be supplied by the alar ligaments and the tectorial membrane 9 (figure 3). The alar ligaments limit axial rotation 23 (figure 7): the failure of the ligament, reported
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The Neuroradiology Journal 20: 209-217, 2007
Figure 8 A-C Coronal diagrams showing from forward to back the numerous ligaments joining the CCJ. The tectorial membrane (TM) is the only elastic ligament present at this level. LL: lateral ligaments reinforcing the atlantooccipital joint capsules (C) very strong in comparison to C1-C2 ones. TL: transverse ligament, the main guide during the rotation of the atlas around the dens.
A
B
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Figure 9 A,B A) Power’s ratio, the ratio obtained dividing the distance B-C (basion-posterior ring of C1) by A-O (distance opisthion-anterior ring of C1) normally equals 1 or is slightly less. A value greater than 1.0 suggests translational anterior dislocation of C0-C1. Ratios approaching 0.7 can occur in case of posterior dislocation, fracture of the dens or congenital narrowing of the occipital foramen. B) Vertical dislocations of the dens can be evaluated by the Wackenheim line in respect to which the dens is located forward and downward, the Chamberlain line (hard palate-opisthion) in respect to which the dens is located between 1mm below and 0.6 mm above it and the McRae line (basion-opisthion), crossed by the dens in case of basilar invagination.
Figure 11 The behaviour of a spinal motion segment can be compared to a ball in a plate or in a wine glass. In a large plate the ball is free to move without resistance having a relatively large NZ. In a normal person the neutral zone is included in the pain-free zone. The opposed conditions eventually promote mechanical pain. From Clark, modified 4. Figure 10 The load-displacement curve of any functional spinal unit is not linear but shows two distinct components: the neutral zone (NZ) with greater compliance at the beginning of the movement and the elastic zone (EZ) with rapid increase in resistance.
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to occur at about 200N 8 provokes a mean increase in contralateral rotation of about 11-30°, equally divided between the occipitoatlantal and atlantoaxial joints 6. The tension of the alar ligaments is also responsible for the forced rotation of C2 during lateral bending 7. The very strong ventral ring of C1 and the transverse and alar ligaments suffice to guide rotation: an intact dorsal ring of C1 is not necessary for stability 3. Instability and Failure of CCJ White amd Panjabi 24 defined “clinical instability” as “the loss of the ability of the spine under physiologic loads to maintain relationships between vertebrae in such a way that there is neither damage nor subsequent irritation to the spinal cord or nerve roots and, in addition, there is no development of incapacitating deformity or pain due to structural changes”. They proposed several radiological criteria for evaluating C0-C1-C2 instability: >8° > 1 mm
axial rotation C0-C1 to one side C0-C1 translation in the sagittal plane > 7 mm overhang C1-C2 (total right and left) > 45° axial rotation C1-C2 to one side > 4 mm C1-C2 translation in the sagittal plane < 13 mm posterior body C2-posterior ring C1 in the sagittal plane Avulsed transverse ligament C0-C1 traumatic instability is most common in childhood 2. In case of C0-C1 instability dislocation can occur in either longitudinal (basilar impression), anterior or posterior directions and can be evaluated through several reference lines between bony landmarks of the base of the skull such as the Power’s ratio (figure 9A) and Wackenheim’s, Chamberlain’s and McRae’s lines (figure 9B). Clinical instability of the C1-C2 joint implies abnormal translation and/or rotation. Rotational C1-C2 displacement can be anterior or posterior, or combined anterior and posterior. In both anterior or posterior forms the vertical rotational axis is displaced on the contralateral joint because of the transverse ligament and dislocated capsule failure, weakness or dens deficiency, respectively. In the combined forms the dens is the axis of an abnormal rotation due to disruption of both capsules. 214
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The classical concepts of instability rely on the association between an overall increase in the range of motion (ROM) and pain and/or neurological deficit. Nevertheless a significant increase in the ROM is actually not present in many clinical and experimental cases of instability. A more sensitive and reliable indicator of instability can be considered the first part of the ROM during which the spine moves opposing the least resistance referred to as the neutral zone (NZ) 16 (figure 10). The behaviour of a spinal segment motion was compared to a ball moving in a plate, having a large NZ, or in a wine glass with vertical borders and a small NZ (figure 11). According to many biomechanical experiments in case of injury or fracture the NZ often increases beforehand and to a greater extent, while in case of surgical fixation it decreases more than the ROM 11,15,22. Panjabi 16 redefined clinical instability as the loss of the ability of the spine to maintain the intervertebral neutral zones within physiological limits. An unstable painful spine would have a NZ larger than the painless zone. The CCJ is prone to injuries because of: – special anatomy; – high mobility; – frequent involvement in head traumas. CCJ traumas are more often fatal than injuries involving the subaxial spine, and are most common in children under 12 in whom they represent up to 83% of cervical injuries 2. Most CCJ injuries result from blows to the head with the next more important mechanism being the sudden deceleration of the body. Several factors determine the type of injur : • energy of vector force; • rate of load application; • direction of the vector force and its point of application; • posture of the head and spine; • intrinsic strength of the bony elements; • displacement. In case of failure producing stress, the kinetic energy mostly influences the magnitude of the injury 28. The rate of loading or deformation is also important because of the viscoelastic behaviour of the spinal bony and soft elements: under increasing rates of loading the varied viscoelasticity causes different changes in the stressstrain curves. The increase in loading rate increases the energy absorption either at the failure point or in surrounding tissues.
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The Neuroradiology Journal 20: 209-217, 2007
A
B
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Figure 12 A,B Influence of the direction and point of application of injuring vector forces in deciding the location of several among the main types of traumas in the sagittal (A) and lateral planes (B). Even slight changes in the vectors provoke fractures totally different in location and prognosis. From Benzel, modified 3.
Figure 14 A,B A possible, but rarer consequence of an axial injuring vector force is the body-peduncle sagittal fracture of C2, favoured by the absence of support of the facets (A). B) A more lateral or oblique injury (figure 12B) dislocates the fracture laterally (B).
Figure 13 A-C Pure axial loads are not of concern for the dens which is not affected at all. The loads are entirely accepted by the lateral masses of C1 ring or the superior facets of C2 with eventual Jefferson or type II burst fracture of the latter (C). A,B) In case of flexion or extension the dens works as a lever arm receiving the forces by the anterior arc of C1 or by the transverse ligament and it creates a bending moment.
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In car accidents the padded surfaces protecting the skull at impact decrease the rate of loading, but at same time can reduce the dissipation of the forces to the shoulders and chest increasing the total energy transmitted to the neck favouring injuries, as proven in tests using cadaver models 14. The direction of the vector force and its point of application are the primary factors determining the location of injury (figure 12). In biomechanical tests even small variations in the orientation and point of application of loads can produce significant variations in the resulting fractures 13. This concept is well illustrated in the diagram in figure 12 showing a simplified uniplanar analysis of the main mechanisms of injuries by vector forces acting in the sagittal and coronal planes. While a horizontal frontal impact causing the sudden isolated extension of the head without any distractive component provokes the classical traumatic spondylolisthesis of the axis (vector B), an oblique impact on the superior forehead, just a few cm above, through an axial loading (vector C) and a slightly less caput extension, shifts the fracture line in the dorsal body (type I) of C2 with subluxation-extension of C2. An even more cranial and oblique load vector (mechanism D) favours the eventual addition of a ventral teardrop C2 fracture, creating a distraction on the ventral C2-C3 interspace. Dorsally applied vector forces tend to cause opposed reactions with C2-C3 dorsal discal space opening and flexion-subluxation of C2 (with eventual dorsal teardrop) in case of combined hyperflexion and axial loading (figure 12A, vector F), or type III dens fracture or transverse ligament disruption in case of pure flexion (figure 12A, vector G) Traumas by pure axial loads on the head vertex are relatively rare (figure 12A,B vector E). In pure axial load the lateral masses of C1 and C2 accept all of the load. The dens is not affected at all. Because of the oblique orientation of the C0-C1 facet joints the vertical vector
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divides into two laterally orientated resultant forces favouring the bursting of C1 ring, the weakest point of the CCJ (figure 13C) or a sagittal vertical body-peduncle fracture (type II) of C2 (figures 13C, 14A). The addition of a lateral component to the vertical loading (figure 12B, vector I) can dislocate the fracture line laterally through the foramina transversaria (figure 14B). In most cases, when axial loads are applied out of the skull vertex or when the head and spine are in flexion or extension posture, a combined hyperflexion or hyperextension are also created for which the energy is delivered to the odontoid process via the anterior arc of C1 or the transverse ligament with the dens acting as a lever arm (figure 13). Sometimes fractures seemingly similar by location can be generated by even opposed mechanisms, as in case of the vertical coronally orientated dorsal (type I) C2 body fractures which can be the result of either a vertical loadinghyperextension (figure 12A, vector C) or a capital hyperflexion-distraction (figure 12A, vector H): in these cases the eventual dislocations are very important indications of the real mechanism. The relative strength of different soft and bony structures also contributes, but secondarily, to establishing the location of injury determining the point/s, “setting the stage” 3 for the energy to be delivered 28. The influence of the intrinsic strength and weakness of the bony and soft components explains why more than one injury can result from a single force vector: for example, a pure axial load applied on the head vertex can result in either a burst fracture of C1 ring (figure 13C), a type I-II occipital condyle fracture, a sagittal body fracture (type II) of C2 (figure 13C) or, finally, a burst fracture of the subaxial cervical spine. Finally, for a given load greater displacements cause more severe cervical injuries: seatbelt restraints and headrests on car seats reduce the daily incidence of severe cervical spine traumas 26,27.
References 1 Afifi AK, Bergman RA: Functional Neuroanatomy: Text and Atlas. McGraw-Hill 1998. 2 Apple JS, Kirks DR, Merten DF et Al: Cervical spine fractures and dislocations in children. Pediatr Radiol 17: 45, 1987. 3 Benzel EC: Biomechanics of the Spine. Thieme-Verlag, Stuttgart 2003 4 Clark R7 The Cervical Spine 3rd Ed. Lippincot-Raven, Philadelphia 1998.
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5 Diano AA: Biomeccanica ed Anatomia della Colonna Vertebrale. Idelson-Gnocchi, Napoli 2003. 6 Dvorak J, Hayek J, Zehnder R: CT-functional diagnostics of the rotatory instability of the upper cervical spine: part 2. An evaluation on healthy adults and patients with suspected instability. Spine 12: 726-731, 1987. 7) Dvorak J, Panjiabi MM: Functional anatomy of the alar ligaments. Spine 12: 183, 1987.
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8 Dvorak J, Schneider E et Al: Biomechanics of the cranio-cervical region: the alar and transverse ligaments. J Orthop Res 6: 452-461, 1988. 9 Fielding LW, Cochran GVB, Lansing JF et Al: Tears of the transverse ligament of the atlas: a clinical biomechanical study. J Bone Joint Surg (Am) 56: 1683, 1974. 10 Goel VK, Clark CR, Galles K, Liu YK: Moment-rotation relationships of the ligamentous occipito-atlantoaxial complex J Biomech 21: 673-680, 1988. 11 Grob D, Dvorak J: Temporary segmental fixation of the cervical spine. Presented at the meeting of European Spine Society. Rome 1991. 12 Hecker P: Appareil ligamenteux occipito-atloido-axoidien:etude d’anatomie compare. Arch Anat Hist Embryol 2: 57-95, 1923. 13 McElhaney JH, Paver JG, McCracklin HJ: Cervical spine compression responses. Proceedings of the 27th STAPP Car Crash Conference, Society of Automotive engineers, Warrendale, PA 1983: 163. 14 Nusholtz GS, Huelke DE, Lux P et Al: Cervical spine injury mechanisms. 27th STAPP Car Crash Conference. Warrendale, PA: Society Of Automotive Engineers 1983: 179-197. 15 Oxland TR, Panjabi MM: The onset and progression of spinal injury: a demonstration of neutral zone sensitivity. J Biomechanics 25: 1165-1172, 1992. 16 Panjabi MM: The stabilizing system of the spine. Part II Neutral zone and instability hypothesis. J Spinal Disord 5: 390-397, 1992. 17 Panjabi MM, Dvorak J, Duranceau J et Al: Three dimensional movements of the upper cervical spine. Spine 13: 726-730, 1988. 18 Panjabi MM, Dvorak J, Sandler A et Al: Cervical Spine Kinematics and Clinical Instability. In Clark CR Ed. The Cervical Spine, Lippincot-Raven. Philadelphia 1998. 19 Penning l, Wilmink JT: Rotation of the cervical spine: A CT study in normal subjects. Spine 12: 732-738, 1987. 20 Rabischong P: Anatomie Functionelle du rachis et de la moelle. In: Imagerie du Rachis et de la Moelle Manelfe C Ed. Vigot. Paris 1989: 109-123.
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21 Rabischong P, Salvolini U: La logica anatomica dell’imaging vertebro-nevrassiale. In: L’imaging Diagnostico del Rachide. Libreria Cortina, Verona 1987. 22 Slosar PJ Jr, Patwardhan A, Lorenz M et Al: Threedimensional instability patterns of the thoracolumbar burst fracture. Trans orthop Res Soc 17: 67, 1992. 23 Werne S: Studies on spontaneous atlas dislocation. Acta Orthop Scand 1957: 23:35. 24 White AA, Panjabi MM: Clinical Biomechanics of the Spine. 2nd edition. Philadelphia: JB Lippincot 1990. 25 Wiesel SW, Rothman RH: Occipito-atlantal hypermobility. Spine 4: 187, 1979. 26 Yoganandan N, Haffner M, Maiman DJ: SAE Technical Paper series. Epidemiology and Injury Biomechanics of otor Vehicle Related Trauma to the Human Spine. 33rd STAPP Car crash Conference Washington, D.C. 1989: 223-242. 27 Yoganandan N, Sances A, Pintar F: Injury biomechanics of the human cervical column. Spine 15: 1031-1039, 1990. 28 Zhu Q, Ouyang J: traumatic instabilities of the cervical spine caused by high-speed axial compression in a human model. Spine 24: 440-444, 1999.
Dr Roberto Izzo Head Neuroradiology CT Neuroradiology Cardarelli Hospital Via Cardarelli, 9 80110 Napoli, Italy Tel.: 081 8599147 home Tel.: 081 7471111 Hospital Cell.: 335 8431259 Dr Roberto Izzo Via Cavalcavia del Sarno, 12 80045 Pompei, Italy E-mail: [email protected]
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Biomechanics of the Spine III. The Cranio-Cervical Junction R. IZZO, G. AMBROSANIO, A. CIGLIANO*, D. CASCONE**, G. GALLO***, M. MUTO Neuroradiology Department A.O.R.N., A. Cardarelli; Napoli, Italy * Emergency Neurosurgery Department A.O.R.N., A. Cardarelli; Napoli, Italy ** Graduate in Medicine, external collaborator *** CDS Portici; Napoli, Italy
Key words: biomechanics, cranial-cervical junction, traumas, spinal instability
SUMMARY – By virtue of its unique anatomy and functions the cranial-cervical junction was excluded in previous reviews on the general biomechanics of the spine, being a world apart. The special design of the cranial-cervical (CCJ) junction responds to seemingly opposed necessities being at same time loose enough to allow a great variety of movements and strong enough to preserve the spinal cord and vertebral arteries and to resist the head weight and muscular action. The primary goal of the CCJ is to ensure the maximal mobility of the head for visual and auditory exploration of space. Like a cardan joint the CCJ allows simultaneous independent movements about three axes in order to repeat and extend eye movements under the control of vestibular receptors. Several muscular groups and a number of ligaments control the movements of the CCJ and ensure its stability. Although composed of two seemingly distinct joints the CCJ forms a unique functional complex whose stability is ensured by ligaments and bony restraints often operating on both joint components: the occipitoatlantal and atlantoaxial joints.
Introduction The Functional Program of the CCJ
The cranial-cervical junction (CCJ) is a transitional structure programmed to ensure maximum mobility of the head for the visual and auditory exploration of space (figure 1). In order to obtain a stereoscopic vision and the fusion of the images coming from both halves of the visual scene the light pulses have to be direct on the maculas which having the highest concentration of cones account for the maximal visual resolution and for as much as 8/10° of visual acuity. For this purpose the co-ordinated action of the orbital muscles performs fine adjustments in a range of about 30° in both horizontal and vertical planes over which the precision of movements fades. A complete exploration of space demands coupled movements of the eyeballs and the head. The co-ordinated activity of the eyes and
the head is a very complex program mainly relying on: – a special fibre tracts association referred to as the medial longitudinal fasciculus (MLF) directly and indirectly, through the reticular formation, connecting the vestibular nuclei, in turn stimulated by the gravity and acceleration receptors of the labyrinths, and extraocular muscles and XI nerve nuclei controlling the eyes, head and neck movements, respectively 1,20,21 . – a special mechanical device: the CCJ allowing the head to perform and extend the same movements as the gaze. All four vestibular nuclei send direct and crossed outputs on III, IV e VI nerve nuclei via ascending components of the MLF with inhibitory and excitatory effects respectively, controlling the conjugate eye movements 1. Like a cardan system, the CCJ realizes two separate degrees of freedom with simultaneous and independent movements about three axes 20,21: 1. flexion-extension around a transversal axis; 209
Biomechanics of the Spine III. The Cranio-Cervical Junction
2. axial rotation around a vertical axis; 3. instantaneous, from the combination of 1 and 2. The one and two axes are fixed, the third is variable. Thanks to the CCJ the neck muscles can perform a great variety of movements at same time attaining a precise control of any single movement. By virtue of its special anatomy the C0-C1-C2 complex allows high freedom of movements being strong enough to preserve the spinal cord and vertebral arteries and to support the head weight and muscle action. Kinematics of the CCJ The occiput-C1-C2 complex as a whole accounts for 40% of all cervical flexion-extension and 60% of global rotation. The average movements performed by two components of the CCJ are summarized in table 1 17,19. Table 1 Movements of the CCJ
Joint
Motion
Range of Motion
C0-C1
flexion-extension lateral bending (unilat.) axial rotation (unilat.)
25° 05° 05°
C1-C2
flexion-extension lateral bending (unilat.) axial rotation (unilat)
15° 05° 40°
The occipitoatlantal joint This joint consists of spherical articulations cobered by tough capsules which contribute to joint stability. The primary movement of the occiput-C1 joint is flexion-extension during which the occipital condyles rotate and move in posterior and anterior directions, respectively 5 (figure 2). Table 2 indicates the elements restraining these movements: Restrainers of Flexion
R. Izzo
During flexion-extension the tectorial membrane and alar ligaments prevent sagittal translation between the basion and the tip of the dens whose range must not exceed 1 mm 23,25 , with a minor stabilising contribution coming from the cup-like facets of C1 (figure 3). About 5° of both axial rotation and lateral bending are also allowed 10,17, both checked by the alar ligaments 7, while axial rotation is also limited by the superior facets of C1 (figure 4). The atlantoaxial joint The C1-C2 joint, the most mobile individual joint of the cervical spine, performs most of the head’s rotation, with the atlas ring pivoting about the dens while the lateral masses slide upon the facets of C2 in opposite directions, favoured by the convexity of the surfaces limiting the reciprocal contact, and by loose capsules (figure 5). Because of the convexity of the articular surfaces C1 descends in relation to the superior facets of C2 during axial rotation. In the subaxial cervical spine the inclination of the facets allows much less axial rotation. Panjabi et Al 18 reported a general tendency to decrease with aging for all movements of the cervical spine, except the axial rotation of the CCJ. According to Rabichong 20,21 axial rotation is performed by two muscular systems: – a profound group composed of the superior and inferior obliqui muscles (SOM) (IOM); – a superficial group with the sternocleidomastoid (SCM), splenius capitis (SCA) and splenius cervicis (SCE) muscles. The IOM performs the first 30°of head rotation with a relatively fine action through its insertions on the transverse process of C1 and the spinous process of C2 (figure 6). This traction, unilateral and not balanced, creates a backwards translation of the atlas ring blocked by the contact with the dens. The movement is therefore continued by the opposed actions of the SCM and SCA whose superior insertions are located laterally on the Restrainers of Extension
Basion-tip of the dens contact
Tectorial membrane tension
posterior atlantooccipital membrane tension capsular tension alar ligaments tension posterior muscles tension oral floor-neck contact
anterior atlantooccipital membrane tension capsular tension occiput-dorsal arc of C1 contact suboccipital muscles compression
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Figure 2 A-C A) During extension of the head the occipital condyles rotate and slide forwards in the cup-shaped superior facets of C1. The opposite movements occur during the flexion (C). The sliding movements are stressed by the varying positions of the red asterisks used as reference points.
Figure 1 Diagram of a coronal section of both C0-C1 and C1-C2 joints. AO: occipitoatlantal joint. AAL: lateral atlantoaxial joint.
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Figure 4 The C0-C1 joint also performs a limited axial rotation, restrained by the cup-shaped facets of C1 in which the occipital condyles have to rise for displacement. From Diano, with permission 5.
Figure 3 Lateral view of the C0-C1-C2 joints. The normal distance between the tip of the dens and the basion is 4 to 5 mm (A). Any change in this gap over 1 mm during the flexionextension of the head with a normal transverse ligament indicates instability of C0-C1 joint. Also important for evaluation are the distances between the dens and the anterior ring of C1 (B) and the anterior cortex of the posterior C1 ring (C).
Figure 5 During the axial rotation of the head the C1-C2 lateral joints slide easy in opposite directions favoured by the convex surfaces reducing the reciprocal contact. At the end of the movement the lateral masses of C1 slightly descend in relation to the superior facets of C2 (vertical arrow). From Diano, with permission 5.
mastoids, while the inferior attachments are near the median line in order to obtain the maximal rotation possible in spite of a twitch capacity of just one-third of muscular length (figure 6) 20,21. The SCM and SCA have a powerful balanced
action. Their oblique orientation creates simultaneous compressive forces having a stabilising role, but also being responsible for mechanical stress and degenerative modifications 20 on the joints below. The alar ligaments’ tension limits the axial rotation 23 (figure 7). 211
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The C1-C2 junction also allows about 15° of flexion-extension restricted by the tectorial membrane and the contact between bony components 17. Stability of the CCJ
Figure 6 The obliquus capitis inferior muscle (IO) performs the first 30°of head rotation via its insertions on the transverse process of C1 and the spinous process of C2. The movement is therefore continued by the opposed actions of the sternocleidomastoid (SCM) and splenius capitis (SCA) muscles located in superficial position. SCE: splenius cervicis muscle.
Figure 7 A-C Diagram of the alar ligaments viewed from above. The alar ligaments are most important in controlling the range of atlas rotation. In neutral position the ligaments are lax. The tension first involves the ligament of the same side of rotation (B), then the contralateral one (C). Their intrinsic strength is very high if compared to loads they must resist. From Clark, modified 4.
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By virtue of its peculiar anatomic and biomechanical features the CCJ has specific patterns of stability completely different from the rest of the spine. Its great mobility demands a number of ligaments to control the movements and ensure stability (figure 8). An important principle in evaluating the stability of the CCJ is that, as discussed for normal movements, many ligaments and bony restraints control and stabilise not just one, but both the C0-C1 and C1-C2 compartments at the same time. In the C0-C1 joint, for example, the work of the intrinsic ligaments, the capsules and the anterior and posterior atlantoocciptal membranes, is flanked by “extrinsic” ligaments connecting the occiput and C2 12: the tectorial membrane, the alar and apical ligaments. The normal distance between the tip of the dens and the basion must be not exceed 45 mm and must never vary more than 1 mm during flexion-extension (figure 3). The most important ligaments ensuring the stability of C1-C2 joint are: - the transverse ligament; - the alar ligaments; - the apical ligament. The transverse ligament, the most important component of the cruciate ligament, avoids the anterior displacement of the atlas during axial rotation guaranteeing the free pivoting of the dens. By virtue of a special lattice arrangement of the collagen fibres the transverse ligament is most resistant to tension, with a failure strength in biomechanical tests ranging from 170 up to 700 N corresponding to about 17 to 70 kg, respectively 8. Any increase over 3 mm of the atlantodental space or reduction below 13 mm of the distance between the posterior surface of the dens and anterior cortical of the posterior ring of C1 can occur only in case of failure of the transverse ligament (with an intact dens) whose action cannot be supplied by the alar ligaments and the tectorial membrane 9 (figure 3). The alar ligaments limit axial rotation 23 (figure 7): the failure of the ligament, reported
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Figure 8 A-C Coronal diagrams showing from forward to back the numerous ligaments joining the CCJ. The tectorial membrane (TM) is the only elastic ligament present at this level. LL: lateral ligaments reinforcing the atlantooccipital joint capsules (C) very strong in comparison to C1-C2 ones. TL: transverse ligament, the main guide during the rotation of the atlas around the dens.
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Figure 9 A,B A) Power’s ratio, the ratio obtained dividing the distance B-C (basion-posterior ring of C1) by A-O (distance opisthion-anterior ring of C1) normally equals 1 or is slightly less. A value greater than 1.0 suggests translational anterior dislocation of C0-C1. Ratios approaching 0.7 can occur in case of posterior dislocation, fracture of the dens or congenital narrowing of the occipital foramen. B) Vertical dislocations of the dens can be evaluated by the Wackenheim line in respect to which the dens is located forward and downward, the Chamberlain line (hard palate-opisthion) in respect to which the dens is located between 1mm below and 0.6 mm above it and the McRae line (basion-opisthion), crossed by the dens in case of basilar invagination.
Figure 11 The behaviour of a spinal motion segment can be compared to a ball in a plate or in a wine glass. In a large plate the ball is free to move without resistance having a relatively large NZ. In a normal person the neutral zone is included in the pain-free zone. The opposed conditions eventually promote mechanical pain. From Clark, modified 4. Figure 10 The load-displacement curve of any functional spinal unit is not linear but shows two distinct components: the neutral zone (NZ) with greater compliance at the beginning of the movement and the elastic zone (EZ) with rapid increase in resistance.
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to occur at about 200N 8 provokes a mean increase in contralateral rotation of about 11-30°, equally divided between the occipitoatlantal and atlantoaxial joints 6. The tension of the alar ligaments is also responsible for the forced rotation of C2 during lateral bending 7. The very strong ventral ring of C1 and the transverse and alar ligaments suffice to guide rotation: an intact dorsal ring of C1 is not necessary for stability 3. Instability and Failure of CCJ White amd Panjabi 24 defined “clinical instability” as “the loss of the ability of the spine under physiologic loads to maintain relationships between vertebrae in such a way that there is neither damage nor subsequent irritation to the spinal cord or nerve roots and, in addition, there is no development of incapacitating deformity or pain due to structural changes”. They proposed several radiological criteria for evaluating C0-C1-C2 instability: >8° > 1 mm
axial rotation C0-C1 to one side C0-C1 translation in the sagittal plane > 7 mm overhang C1-C2 (total right and left) > 45° axial rotation C1-C2 to one side > 4 mm C1-C2 translation in the sagittal plane < 13 mm posterior body C2-posterior ring C1 in the sagittal plane Avulsed transverse ligament C0-C1 traumatic instability is most common in childhood 2. In case of C0-C1 instability dislocation can occur in either longitudinal (basilar impression), anterior or posterior directions and can be evaluated through several reference lines between bony landmarks of the base of the skull such as the Power’s ratio (figure 9A) and Wackenheim’s, Chamberlain’s and McRae’s lines (figure 9B). Clinical instability of the C1-C2 joint implies abnormal translation and/or rotation. Rotational C1-C2 displacement can be anterior or posterior, or combined anterior and posterior. In both anterior or posterior forms the vertical rotational axis is displaced on the contralateral joint because of the transverse ligament and dislocated capsule failure, weakness or dens deficiency, respectively. In the combined forms the dens is the axis of an abnormal rotation due to disruption of both capsules. 214
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The classical concepts of instability rely on the association between an overall increase in the range of motion (ROM) and pain and/or neurological deficit. Nevertheless a significant increase in the ROM is actually not present in many clinical and experimental cases of instability. A more sensitive and reliable indicator of instability can be considered the first part of the ROM during which the spine moves opposing the least resistance referred to as the neutral zone (NZ) 16 (figure 10). The behaviour of a spinal segment motion was compared to a ball moving in a plate, having a large NZ, or in a wine glass with vertical borders and a small NZ (figure 11). According to many biomechanical experiments in case of injury or fracture the NZ often increases beforehand and to a greater extent, while in case of surgical fixation it decreases more than the ROM 11,15,22. Panjabi 16 redefined clinical instability as the loss of the ability of the spine to maintain the intervertebral neutral zones within physiological limits. An unstable painful spine would have a NZ larger than the painless zone. The CCJ is prone to injuries because of: – special anatomy; – high mobility; – frequent involvement in head traumas. CCJ traumas are more often fatal than injuries involving the subaxial spine, and are most common in children under 12 in whom they represent up to 83% of cervical injuries 2. Most CCJ injuries result from blows to the head with the next more important mechanism being the sudden deceleration of the body. Several factors determine the type of injur : • energy of vector force; • rate of load application; • direction of the vector force and its point of application; • posture of the head and spine; • intrinsic strength of the bony elements; • displacement. In case of failure producing stress, the kinetic energy mostly influences the magnitude of the injury 28. The rate of loading or deformation is also important because of the viscoelastic behaviour of the spinal bony and soft elements: under increasing rates of loading the varied viscoelasticity causes different changes in the stressstrain curves. The increase in loading rate increases the energy absorption either at the failure point or in surrounding tissues.
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Figure 12 A,B Influence of the direction and point of application of injuring vector forces in deciding the location of several among the main types of traumas in the sagittal (A) and lateral planes (B). Even slight changes in the vectors provoke fractures totally different in location and prognosis. From Benzel, modified 3.
Figure 14 A,B A possible, but rarer consequence of an axial injuring vector force is the body-peduncle sagittal fracture of C2, favoured by the absence of support of the facets (A). B) A more lateral or oblique injury (figure 12B) dislocates the fracture laterally (B).
Figure 13 A-C Pure axial loads are not of concern for the dens which is not affected at all. The loads are entirely accepted by the lateral masses of C1 ring or the superior facets of C2 with eventual Jefferson or type II burst fracture of the latter (C). A,B) In case of flexion or extension the dens works as a lever arm receiving the forces by the anterior arc of C1 or by the transverse ligament and it creates a bending moment.
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In car accidents the padded surfaces protecting the skull at impact decrease the rate of loading, but at same time can reduce the dissipation of the forces to the shoulders and chest increasing the total energy transmitted to the neck favouring injuries, as proven in tests using cadaver models 14. The direction of the vector force and its point of application are the primary factors determining the location of injury (figure 12). In biomechanical tests even small variations in the orientation and point of application of loads can produce significant variations in the resulting fractures 13. This concept is well illustrated in the diagram in figure 12 showing a simplified uniplanar analysis of the main mechanisms of injuries by vector forces acting in the sagittal and coronal planes. While a horizontal frontal impact causing the sudden isolated extension of the head without any distractive component provokes the classical traumatic spondylolisthesis of the axis (vector B), an oblique impact on the superior forehead, just a few cm above, through an axial loading (vector C) and a slightly less caput extension, shifts the fracture line in the dorsal body (type I) of C2 with subluxation-extension of C2. An even more cranial and oblique load vector (mechanism D) favours the eventual addition of a ventral teardrop C2 fracture, creating a distraction on the ventral C2-C3 interspace. Dorsally applied vector forces tend to cause opposed reactions with C2-C3 dorsal discal space opening and flexion-subluxation of C2 (with eventual dorsal teardrop) in case of combined hyperflexion and axial loading (figure 12A, vector F), or type III dens fracture or transverse ligament disruption in case of pure flexion (figure 12A, vector G) Traumas by pure axial loads on the head vertex are relatively rare (figure 12A,B vector E). In pure axial load the lateral masses of C1 and C2 accept all of the load. The dens is not affected at all. Because of the oblique orientation of the C0-C1 facet joints the vertical vector
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divides into two laterally orientated resultant forces favouring the bursting of C1 ring, the weakest point of the CCJ (figure 13C) or a sagittal vertical body-peduncle fracture (type II) of C2 (figures 13C, 14A). The addition of a lateral component to the vertical loading (figure 12B, vector I) can dislocate the fracture line laterally through the foramina transversaria (figure 14B). In most cases, when axial loads are applied out of the skull vertex or when the head and spine are in flexion or extension posture, a combined hyperflexion or hyperextension are also created for which the energy is delivered to the odontoid process via the anterior arc of C1 or the transverse ligament with the dens acting as a lever arm (figure 13). Sometimes fractures seemingly similar by location can be generated by even opposed mechanisms, as in case of the vertical coronally orientated dorsal (type I) C2 body fractures which can be the result of either a vertical loadinghyperextension (figure 12A, vector C) or a capital hyperflexion-distraction (figure 12A, vector H): in these cases the eventual dislocations are very important indications of the real mechanism. The relative strength of different soft and bony structures also contributes, but secondarily, to establishing the location of injury determining the point/s, “setting the stage” 3 for the energy to be delivered 28. The influence of the intrinsic strength and weakness of the bony and soft components explains why more than one injury can result from a single force vector: for example, a pure axial load applied on the head vertex can result in either a burst fracture of C1 ring (figure 13C), a type I-II occipital condyle fracture, a sagittal body fracture (type II) of C2 (figure 13C) or, finally, a burst fracture of the subaxial cervical spine. Finally, for a given load greater displacements cause more severe cervical injuries: seatbelt restraints and headrests on car seats reduce the daily incidence of severe cervical spine traumas 26,27.
References 1 Afifi AK, Bergman RA: Functional Neuroanatomy: Text and Atlas. McGraw-Hill 1998. 2 Apple JS, Kirks DR, Merten DF et Al: Cervical spine fractures and dislocations in children. Pediatr Radiol 17: 45, 1987. 3 Benzel EC: Biomechanics of the Spine. Thieme-Verlag, Stuttgart 2003 4 Clark R7 The Cervical Spine 3rd Ed. Lippincot-Raven, Philadelphia 1998.
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5 Diano AA: Biomeccanica ed Anatomia della Colonna Vertebrale. Idelson-Gnocchi, Napoli 2003. 6 Dvorak J, Hayek J, Zehnder R: CT-functional diagnostics of the rotatory instability of the upper cervical spine: part 2. An evaluation on healthy adults and patients with suspected instability. Spine 12: 726-731, 1987. 7) Dvorak J, Panjiabi MM: Functional anatomy of the alar ligaments. Spine 12: 183, 1987.
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8 Dvorak J, Schneider E et Al: Biomechanics of the cranio-cervical region: the alar and transverse ligaments. J Orthop Res 6: 452-461, 1988. 9 Fielding LW, Cochran GVB, Lansing JF et Al: Tears of the transverse ligament of the atlas: a clinical biomechanical study. J Bone Joint Surg (Am) 56: 1683, 1974. 10 Goel VK, Clark CR, Galles K, Liu YK: Moment-rotation relationships of the ligamentous occipito-atlantoaxial complex J Biomech 21: 673-680, 1988. 11 Grob D, Dvorak J: Temporary segmental fixation of the cervical spine. Presented at the meeting of European Spine Society. Rome 1991. 12 Hecker P: Appareil ligamenteux occipito-atloido-axoidien:etude d’anatomie compare. Arch Anat Hist Embryol 2: 57-95, 1923. 13 McElhaney JH, Paver JG, McCracklin HJ: Cervical spine compression responses. Proceedings of the 27th STAPP Car Crash Conference, Society of Automotive engineers, Warrendale, PA 1983: 163. 14 Nusholtz GS, Huelke DE, Lux P et Al: Cervical spine injury mechanisms. 27th STAPP Car Crash Conference. Warrendale, PA: Society Of Automotive Engineers 1983: 179-197. 15 Oxland TR, Panjabi MM: The onset and progression of spinal injury: a demonstration of neutral zone sensitivity. J Biomechanics 25: 1165-1172, 1992. 16 Panjabi MM: The stabilizing system of the spine. Part II Neutral zone and instability hypothesis. J Spinal Disord 5: 390-397, 1992. 17 Panjabi MM, Dvorak J, Duranceau J et Al: Three dimensional movements of the upper cervical spine. Spine 13: 726-730, 1988. 18 Panjabi MM, Dvorak J, Sandler A et Al: Cervical Spine Kinematics and Clinical Instability. In Clark CR Ed. The Cervical Spine, Lippincot-Raven. Philadelphia 1998. 19 Penning l, Wilmink JT: Rotation of the cervical spine: A CT study in normal subjects. Spine 12: 732-738, 1987. 20 Rabischong P: Anatomie Functionelle du rachis et de la moelle. In: Imagerie du Rachis et de la Moelle Manelfe C Ed. Vigot. Paris 1989: 109-123.
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21 Rabischong P, Salvolini U: La logica anatomica dell’imaging vertebro-nevrassiale. In: L’imaging Diagnostico del Rachide. Libreria Cortina, Verona 1987. 22 Slosar PJ Jr, Patwardhan A, Lorenz M et Al: Threedimensional instability patterns of the thoracolumbar burst fracture. Trans orthop Res Soc 17: 67, 1992. 23 Werne S: Studies on spontaneous atlas dislocation. Acta Orthop Scand 1957: 23:35. 24 White AA, Panjabi MM: Clinical Biomechanics of the Spine. 2nd edition. Philadelphia: JB Lippincot 1990. 25 Wiesel SW, Rothman RH: Occipito-atlantal hypermobility. Spine 4: 187, 1979. 26 Yoganandan N, Haffner M, Maiman DJ: SAE Technical Paper series. Epidemiology and Injury Biomechanics of otor Vehicle Related Trauma to the Human Spine. 33rd STAPP Car crash Conference Washington, D.C. 1989: 223-242. 27 Yoganandan N, Sances A, Pintar F: Injury biomechanics of the human cervical column. Spine 15: 1031-1039, 1990. 28 Zhu Q, Ouyang J: traumatic instabilities of the cervical spine caused by high-speed axial compression in a human model. Spine 24: 440-444, 1999.
Dr Roberto Izzo Head Neuroradiology CT Neuroradiology Cardarelli Hospital Via Cardarelli, 9 80110 Napoli, Italy Tel.: 081 8599147 home Tel.: 081 7471111 Hospital Cell.: 335 8431259 Dr Roberto Izzo Via Cavalcavia del Sarno, 12 80045 Pompei, Italy E-mail: [email protected]
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