The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 86, Issue 3

Scientific Articles | March 01, 2004

Stability Analysis of Craniovertebral Junction Fixation Techniques

Christian M. Puttlitz, PhD¹; Robert P. Melcher, MD²; Frank S. Kleinstueck, MD¹; Juergen Harms, MD²; David S. Bradford, MD¹; Jeffrey C. Lotz, PhD¹

¹ Department of Orthopaedic Surgery, University of California at San Francisco, 1001 Potrero Avenue, Room 3A36, San Francisco, CA 94110. E-mail address for C.M. Puttlitz: puttlit@itsa.ucsf.edu
² Department of Orthopaedics and Traumatology, Center for Spinal Surgery, Klinikum Karlsbad-Langensteinbach Guttmannstrassel, 76307 Karlsbad-Langensteinbach, Germany

View Disclosures and Other Information

In support of their research or preparation of this manuscript, one or more of the authors received grants or outside funding from DePuy AcroMed, Inc. None of the authors received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

Investigation performed at the Department of Orthopaedic Surgery, University of California at San Francisco, San Francisco, California

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J Bone Joint Surg Am, 2004 Mar 01;86(3):561-568

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Abstract

Background: Craniovertebral arthrodesis in the upper cervical spine is challenging because of the high degree of mobility afforded by this region. A novel method for achieving atlantoaxial fixation with use of polyaxial screws inserted bilaterally into the lateral masses of C1 and transpedicularly into C2 with longitudinal rod connection has recently been introduced. The question remains as to whether this technique provides adequate stability when extended cephalad to include the occiput. The purpose of this study was to determine the primary stability afforded by this novel construct and compare its stability with the current standard of bilateral longitudinal plates combined with C1-C2 transarticular screws.

Methods: We used ten fresh-frozen human cadaveric cervical spines (C0-C4). Pure moment loads were applied to the occiput, and C4 was constrained during the testing protocol. We evaluated four conditions: (1) intact, (2) destabilized by means of complete odontoidectomy, (3) stabilization with longitudinal plates with C1-C2 transarticular screw fixation, and (4) stabilization with a posterior rod system with C1 lateral mass screws and C2 pedicle screws. Rigid-body three-dimensional rotations were detected by stereophotogrammetry by means of a three-camera system with use of marker triads. The range of motion data (C0-C2) for each fixation scenario was calculated, and a statistical analysis was performed.

Results: Destabilization of the specimen significantly increased C0-C2 motion in both flexion-extension and lateral bending (p < 0.05). Both fixation constructs significantly reduced motion in the destabilized spine by over 90% for all motions tested (p < 0.05). No significant differences were detected between the two constructs in any of the three rotational planes.

Conclusions: Both hardware systems provide equivalent construct stability in the immediate postoperative period when it is critical for the eventual success of a craniovertebral arthrodesis. On the basis of this work, we believe that the decision to use either construct should be determined by clinical rather than biomechanical concerns.

Figures in this Article

Surgical management of craniovertebral instability usually involves arthrodesis of the occiput and the cervical spine. It is commonly held that the reduction or elimination of motion across fixed spinal segments increases the opportunity for fusion. Achievement of a successful fusion when the craniovertebral junction (C0-C2) is involved is complicated because of the relatively high range of motion across these segments¹. In addition, the complex arrangement of the neurovascular anatomy in the upper cervical spine further confounds certain technical aspects of hardware implantation.

In the past decade, numerous constructs have been developed in order to increase stability and facilitate implantation of the hardware^2-12. Open surgical stabilization of the craniocervical region was initially performed with use of simple bone-graft onlay techniques and was subsequently combined with posterior wiring across the craniovertebral junction^13-16. These constructs evolved to include wiring of both the cervical and occipital regions to contoured rods and pins^9,11,17-19. Despite the fact that most of these patients were managed with additional postoperative immobilization (such as a Minerva cast or halo vest), many of the rod constructs resulted in unsatisfactory failure rates (up to 30%²⁰).

Most contemporary methods use screw fixation in both the occiput and cervical regions with bilateral longitudinal plates or rods. Higher rates of occipitocervical fusion have been reported with use of these more rigid constructs^21-24. The Magerl technique (C1-C2 transarticular screws) has become a standard for attaining atlantoaxial fixation. In order to achieve craniovertebral fixation, these screws are coupled to longitudinal plates that extend superiorly and are attached to the occiput. This technique provides a relatively high degree of construct stability²⁵ and, accordingly, reduces the number of vertebral segments that must be incorporated into the arthrodesis. Although C1-C2 transarticular screw fixation results in a rigid construct, placement of the screws across the atlantoaxial level is highly technical and includes a substantial risk of vertebral artery violation²⁶.

A novel technique for achieving atlantoaxial fixation, which utilizes direct fixation of polyaxial screws to the lateral masses of C1 and through the pedicle of C2, with connection by means of longitudinal rods, has recently been reported²⁷. The proposed advantages of this technique compared with the use of C1-C2 transarticular screws are a reduced risk of vertebral artery insult and the ability to perform reduction maneuvers after individual screw placement in C1 and C2. Extension of the construct to the occiput to achieve craniovertebral fusion has provided excellent preliminary clinical results. However, we know of no biomechanical studies that have documented and compared the stability afforded by cephalad extension of the C1-C2 technique to include the occiput. Thus, the purpose of this study was to investigate and compare the occipitocervical construct stability afforded by this novel screw-rod construct with that of the more commonly used C1-C2 transarticular screw-plate method and wiring techniques.

Materials and Methods

Materials and Methods | Results | Discussion | References

Ten fresh-frozen human cadaveric cervical spines (C0-C4; mean age at the time of death, 67.7 years) were used in this study. Each specimen was evaluated for osseous deformity and alignment with use of anteroposterior and sagittal plane radiographs. Specimens were stored in double plastic bags at —20°C until ready for preparation and/or testing. All soft tissues were removed from the specimen, with care taken to preserve the joint capsules, ligaments, and osseous structures. The fourth cervical vertebra was potted in polymethylmethacrylate such that the midsagittal plane of the C3-C4 disc was kept in a horizontal orientation¹.

The C1-C2 transarticular screw-plate construct (C1-C2 plate; Sofamor Danek, Memphis, Tennessee) consisted of bilateral longitudinal plates with several holes to accommodate the transarticular screws, a smooth region without holes where most of the bending for the craniocervical angle can be performed, and a semicircle-shaped occipital portion with holes for occipital screw attachment (Fig. 1). Occipital attachment was achieved with use of two 6 or 8-mm-long screws for each plate. Transarticular screws were inserted across the atlantoaxial joint according to the original description by Magerl and Seemann²⁸. Before screw placement, proper screw trajectory was verified, with use of Kirschner wires, on sagittal plane radiographs. Screw tightening simultaneously fixed the atlantoaxial joint and the plate to the spine.

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Fig. 1: Cadaveric models (A and C) and radiographs (B and D) of the transarticular screw-plate (A and B) and the polyaxial screw-rod (C and D) constructs. Note the absence of the odontoid process (arrows in B and D) for each fixation scenario.

The posterior screw-rod fixation (C1-C2 rod) was achieved with use of bilateral longitudinal rods that spanned an occipital plate, lateral mass screws in C1, and pedicle screws in C2 (see Fig. 1). A T-shaped plate was fixed to the occiput with use of two midline screws and two more laterally placed screws (6 to 12 mm in length) between the inferior and superior nuchal lines. The plate allowed for variable placement of the rod attachment in the medial-lateral direction. Polyaxial screws (3.5 mm in diameter) with an 8-mm unthreaded upper portion were inserted bilaterally into the lateral masses of C1 with the entry point located in the middle of the confluence of the posterior arch and the inferior aspect of the lateral mass of C1. The trajectory for placement of transpedicular screws in C2 was oriented as described by Ebraheim et al.²⁹. After alignment of the atlantoaxial joints, the rods (3.0 mm in diameter) were fixed with locking nuts to the occipital plate and the screws in the atlas and axis.

We evaluated stability by determining the moment-rotation relationships for each construct. Pure moment loads were applied with use of a system of weights, pulleys, nylon strings, and rods (Fig. 2). Two loading rods were drilled through the skull. A medial-lateral rod extended through the petrous portion of the temporal bone, and an anterior-posterior rod was drilled under the sella turcica. Moments were applied in flexion and extension, lateral bending to both sides, and left and right axial rotation, up to 1.5 N-m after three preconditioning cycles³⁰. Stereophotogrammetry was used to determine three-dimensional displacements of the vertebral levels during pure moment loading. Marker triads were attached to the occiput, C1, C2, and C3. Rigid-body motion was detected with use of a three-camera system (Motion Analysis, Santa Rosa, California). In previous experiments in our laboratory, it was determined that this measurement system is accurate to within ±0.05°. Intervertebral rotations were calculated as Euler angles, and the range of motion for each fixation scenario was determined from the greatest moment load (1.5 N-m).

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Fig. 2: Schema of the experimental apparatus and measurement system. Pure moments were applied to the occiput with use of a system of weights, strings, and pulleys. The resultant motion was detected with use of a three-camera system that tracked rigid-body displacements of marker triads.

Each specimen was tested in its intact condition and after destabilization. Destabilization of the specimen was achieved by removing the odontoid process through the foramen magnum. Odontoidectomy has been used by previous investigators to introduce instability to the C0-C2 region^31,32. Because screw trajectories from either fixation scenario would intersect, providing less purchase for the second system, each specimen was assigned to one of the two occipital fixation groups described above (C1-C2 rod or C1-C2 plate), providing five specimens for each construct.

Statistical analysis was performed with use of a one-way analysis of variance (a = 0.05). Individual differences between groups were delineated with use of the Fisher protected least-significant difference post hoc test for multiple comparisons (SigmaStat 2.0; Jandel Scientific, Chicago, Illinois). Thus, we tested each specimen in flexion-extension, lateral bending, and axial rotation to determine the moment-induced motion in the intact, destabilized, and reconstructed conditions. The data are presented as total motion across the craniovertebral junction (C0-C2) and the adjacent, subaxial level (C2-C3).

Results

Materials and Methods | Results | Discussion | References

Flexion-Extension Stability

Flexion-extension total motion for the intact C0-C2 segments was a mean (and standard error) of 52.0° ± 3.5° at a flexion-extension moment of ±1.5 N-m. Destabilization by means of odontoidectomy significantly (p < 0.01) increased this motion to a mean of 69.7° ± 4.4°. Both fixation methods were able to significantly reduce flexion-extension motion compared with the destabilized condition (p < 0.01) (Fig. 3). These motion reductions were also significant compared with the intact condition. Specifically, the C1-C2 plate and C1-C2 rod constructs permitted approximately 3.5% of the total flexion-extension motion afforded by the destabilized construct. No significant difference was found between the total flexion-extension motion of the two constructs (p = 0.98).

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Fig. 3: The mean range of motion (and standard error) of the C0-C2 segments in flexion-extension for the intact (INT) and destabilized (DS) conditions and for the two fixation constructs. The asterisk indicates a significant difference with respect to the destabilized condition (p < 0.05).

Flexion-extension motion across the adjacent segment (C2-C3) was increased by 60% after removal of the odontoid process, although this change was not significant (p = 0.21) (Fig. 4). Placement of the C1-C2 rod system on the destabilized spine restored the adjacent segment sagittal motion to that of the intact condition (p = 0.98). The C1-C2 plate system reduced the mean motion at C2-C3 below the normal or intact level; however, this motion reduction was not significant (p = 0.35).

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Fig. 4: The mean range of motion (and standard error) in the C2-C3 adjacent segment for the intact (INT) and destabilized (DS) conditions and for the two fixation constructs for all three planes of rotation.

Lateral Bending Motion

Total lateral bending motion at ±1.5 N-m of lateral bending moment for the intact condition was a mean (and standard error) of 23.6° ± 3.0°. Removal of the odontoid process significantly increased (p < 0.01) lateral bending motion to a mean of 33.9° ± 8.3°. Once again, application of both constructs to the destabilized spine resulted in significant motion reductions (p < 0.01) (Fig. 5). The C1-C2 plate reduced total lateral bending motion to a mean of 1.3° ± 0.3°. After application of the C1-C2 rod construct, the total lateral bending motion was a mean of 2.4° ± 1.1°. The difference in motion reduction between the two constructs was not significant (p = 0.81).

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Fig. 5: The mean range of lateral bending motion (and standard error) of the C0-C2 segment for the intact (INT) and destabilized (DS) conditions and for the two fixation constructs. The asterisk indicates a significant difference with respect to the destabilized condition (p < 0.05).

Motion at the adjacent level (C2-C3) was affected by application of the C1-C2 plate system. This construct reduced C2-C3 motion with respect to both the destabilized condition and the C1-C2 rod construct (see Fig. 4); however, these motion differences were not significant (p = 0.06 for both conditions). Both destabilization and the C1-C2 rod constructs increased motion compared with the intact condition; however, these increases were not found to be significant.

Axial Rotation Motion

The intact C0-C2 axial rotation motion at ±1.5 N-m of axial torque was a mean (and standard error) of 82.1° ± 4.7°. Destabilization did not significantly increase axial rotation (mean, 86.7° ± 3.8°). However, application of both the C1-C2 plate and C1-C2 rod systems produced equivalent motion reductions to a mean of 2.6° ± 1.0° and 2.6° ± 1.2°, respectively, across the craniovertebral junction (Fig. 6). These changes were significant with respect to both the intact and destabilized conditions (p < 0.01 for both fixation techniques).

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Fig. 6: The mean range of motion (and standard error) of the C0-C2 segement in axial rotation for the intact (INT) and destabilized (DS) conditions and for the two fixation constructs. The asterisk indicates a significant difference with respect to the destabilized condition (p < 0.05).

The C1-C2 plate hardware demonstrated lower axial rotation range of motion across the adjacent segment than did the intact, destabilized, and C1-C2 rod conditions, although these differences were not significant (p > 0.08 for all conditions). Both the destabilized and C1-C2 rod conditions demonstrated greater axial rotation than did the intact spine, although the difference was not significant (see Fig. 4).

Discussion

Materials and Methods | Results | Discussion | References

We used a cadaver model loaded by pure moments in order to evaluate the construct stability afforded by two upper cervical hardware systems. The data for combined motion in C0-C1 and C1-C2 from the intact condition indicate that our model is comparable with other models that have used this testing technique^30-32. Specifically, we found that the craniovertebral junction (C0-C2) flexion-extension motion, lateral bending motion, and axial rotation was 52.0°, 23.6°, and 82.1°, respectively. Total flexion-extension motion has been reported to range from a mean of approximately 50° to 61°^30,33-36. Panjabi et al.³⁰, using 1.5-N-m pure moment loading, reported mean total C0-C2 lateral bending motion to be 24.4°. Axial rotation, which occurs predominantly at the atlantoaxial level, has been reported to occur across the C0-C2 segment and to range from a mean of 72.4° to 92.2°^30-35. Thus, the current protocol reproduced physiologic ranges of motion in all three planes and allowed us to compare our results with those reported previously for other constructs. In addition, removal of the odontoid produced significant increases in sagittal and frontal plane rotation, which is consistent with the findings in previously published investigations that have used this procedure to impart severe instability to the craniovertebral junction^31,32.

The data indicated equivalence between the two constructs with respect to the achievement of an acute reduction of motion in a destabilized spine. Both constructs significantly reduced motion in the destabilized spine by >90% for all motions tested. This finding is important because the decision to use either construct shifts from initial concerns about stability to other clinical considerations, such as surgical efficacy and technique. Both constructs, although similar with respect to the amount of stability achieved, are different in terms of their surgical implantation. Using a plate system, the surgeon must accomplish the plate-contouring first, followed by fixation of the various vertebral levels to the plate. Individual screw placement is limited by the predrilled holes in the plate, further restricting the possibility for additional compression or distraction to be applied after the hardware is placed. Placement of the C1-C2 transarticular screws can be technically demanding and requires maintenance of atlantoaxial joint reduction during the procedure. Finally, the proper entry point and trajectory of the C1-C2 screws may be difficult or impossible to access in a severely kyphotic patient. Conversely, the rod system allows for independent placement of the screws in C1, C2, and the occipital plate. A reduction maneuver, if necessary, can be performed after the screws and occipital plate are fixed. Each rod can be individually contoured to fit the alignment achieved by the reduction maneuver. The system also allows for application of either distraction or compression forces by means of the screws. Finally, the medial and more cephalad placement of the C2 screws reduces the opportunity for vertebral artery damage.

Differences in occipital fixation were also delineated during the course of this investigation. The more lateral attachment of the longitudinal plates to the occiput resulted in visible perforations of the inner table of the skull, even when the shortest available screws were used, demonstrating the reduction in osseous thickness in these regions^37,38. In contrast, the T-shaped plate allows for a solid midline fixation with use of blunt-ended screws of 10 or 12 mm in length. Two additional screws were fixed immediately lateral to the midline close to the superior nuchal line, an area that has been reported to be an ideal site for occipital screw purchase³⁷.

One important aspect of our model was the inclusion of an adjacent level (C3) that was not part of the affected area (C0-C2). This allowed us to determine not only how destabilization and fixation influenced the area to be fused but also how spinal kinetics would be affected on a more global scale. The data consistently showed that the C1-C2 plate construct tended to reduce motion across the C2-C3 joint (as compared with both the intact and destabilized conditions). Conversely, C2-C3 motion with the C1-C2 rod construct more closely approximated that seen in the intact condition for flexion-extension and axial rotation. One possible explanation for this observation could be that the plate actually provides a motion hindrance of the C2-C3 facet joint by overhanging or covering the C2-C3 facet joint. This is most likely an iatrogenic effect produced by a combination of the relatively cephalad trajectory of the transarticular screw and its entry point, which is situated in proximity to this joint. Impingement of the adjacent facet joint associated with posterior plates in the cervical spine has been previously described. In a series of twenty-nine patients who had combined anteroposterior locking screw-plate fixation for the treatment of traumatic cervical instability, Whitecloud et al.³⁹ found that the posterior plates impinged on the adjacent facet joints in twenty-four patients.

It has been shown that levels adjacent to the fusion mass in the spine are at increased risk for degeneration because of aberrant changes in the spinal loading profile. This has important clinical consequences in the cervical spine because one indication for upper cervical arthrodesis is advanced degenerative changes (such as rheumatoid arthritis). Nonphysiologic motion at adjacent levels due to hardware implantation could increase the rate of degeneration in spines with preexisting degenerative changes at the subaxial levels. Interestingly, according to our data, these adjacent subaxial effects may occur in spines that have been fused or, conversely, in those that have been destabilized. The data indicate that destabilization not only created significant instability in the craniovertebral junction but also resulted in increased C2-C3 intervertebral motion. Restrictions (in the case of fusion) or laxity (instability) of C0-C2 intervertebral motion seem to upset the delicate kinematic and force balance in the craniovertebral junction, resulting in an increased burden on the immediate subaxial level. The change in spinal loading is most likely manifested as increased motion at the C2-C3 level, and it provides a plausible explanation for the higher intervertebral rotations measured across this segment in the present study.

The results of this investigation should be kept within the context of its limitations. We chose to use different cadavera for testing each instrumentation system. This was necessary because of the different screw trajectories used by the two different hardware systems. These trajectories would have intersected one another, possibly reducing the screw purchase of the second system tested. This resulted in a sample size of five for each construct, which clearly reduces the power of our statistical analysis. However, because these two systems provided equivalent mechanical stability and very significant motion reductions with respect to the intact and destabilized conditions, we believe that additional specimens would have only confirmed the C0-C2 results demonstrated with the current series of specimens. It is possible that greater numbers of specimens would have resulted in more statistical significance with respect to the differences in motion seen at the adjacent level (C2-C3). Finally, the current testing protocol allows us to comment on and predict in vivo performance only with respect to acute stability. Fatigue testing is warranted to investigate the time-dependent behavior of either system with respect to loosening or cyclic material failure.

Overall, our data indicate that a construct consisting of C1 and C2 polyaxial screws, occipital screws, and longitudinal rods demonstrates acute mechanical equivalence to a system that utilizes C1-C2 transarticular screws, occipital screws, and longitudinal plates. Each construct was capable of significantly reducing motion in a severely destabilized craniovertebral cadaver model. The decision to use either construct should be made on the basis of the surgical technique and not the acute biomechanical stability.

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Topics

bone plates ; bone screws ; computers ; muscle rigidity ; odontoid process of axis ; range of motion ; rod photoreceptors ; spine ; cervical spine ; equivalent weight

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Atul Goel

Posted on March 31, 2004

Cranio-vertebral Fixation Techniques

Seth G.S. Medical College & KEM Hospital

To The Editor:

We read the above-mentioned manuscript with considerable concern and we wish to bring to your notice certain facts. In 2001, Harms and Melcher published a paper on C1-2 fixation using individual fixation of Cl lateral mass and C2 pedicle with screw and rods (1). They described this technique of fixation as new and novel.

We had brought to the attention of the journal Spine (2) that we were the first to describe this technique and have used this method since 1987. Our experience now exceeds 300 cases during the last 16 years. We have multiple publications on this subject since 1994 indexed in Medline (3- 7,9) as well as in a textbook (8). Harms and Melcher chose not to respond to our letter, which was subsequently published in Spine without the authors' reply (2).

We are surprised to note that in this paper, the authors still label this method as novel and new. The only difference in the present manuscript is that the authors have made a passing reference to our papers; which was missing in their earlier paper published in Spine (1). If there is any difference in their technique when compared to ours, it is that Harms and Melcher have used a commercially made rod instead of the custom made plates that we use.

We have previously described the importance and relevance of sectioning of the C2 ganglion for wide exposure of the region; the opening up of the atlantoaxial facet joint and denuding the articular cartilage; and impacting bone graft into the joint space to provide stability to the construct and enhance ultimate bone fusion. In the present paper the authors have used an extension of C 1-2 fixation by our technique and included the occipital bone in the fixation construct. We also have described this construct in 1994 (7) and subsequently in 1995 (3) and 1997 (8). All these presentations have line drawings and case illustrations demonstrating the technique and its use in a variety of clinical conditions.

We strongly believe that such omissions and misrepresentation of facts are against the norms of intellectual honesty and compromise scientific validity. Nevertheless, we are happy to read this well-structured manuscript, which validates our clinical experience and shows that the construct based on our concepts has sufficient biomechanical strength.

Prof Atul Goel Dr Arvind G. Kulkarni

References I .Harms J, Melcher P. Posterior C 1-C2 Fusion with Polyaxial Screw and Rod Fixation. Spine 2001;26: 2467-71. 2.Goel A, Laheri V. Posterior C1-C2 Fusion with Polyaxial Screw and Rod Fixation. (Letter). Spine 2002;27:1589-1590 3.Goe1 A, Achawal S. Surgical treatment for Arnold Chiari malformation associated with atlantoaxial dislocation. Br J Neurosurg 1. 995; 9: 67-72. 4.Goel A, Gupta S. Vertebral artery injury with transarticular screws [letter]. J Neurosurg 1999; 90: 376-7. 5.Goel A, Gupta S. Quantitative anatomy of the lateral masses of atlas and axis. Neurol India 2000; 48: 120-5. 6.Goel A, Laheri VK. Plate and screw fixation for atlanto-axial dislocation [technical report]. Acta Neurochir (Wien) 1994; 129: 47-53. 7.Goe1 A., Muzumdar D, Dindorkar K, et al. Atlantoaxial dislocation associated with stenosis of canal at atlas. J Postgrad Med 1997; 43: 75-7. 8.Goel A, Kobayashi S. Cramovertebral and spinal stability. In: Kobayashi S, Goel A, Hongo K (eds). Neurosurgery of Complex Tumors and Vascular Lesions. New York: Churchill Livingstone, 1997: 339-72. 9.Goel A, Desai KI, Muzumdar DP. Atlantoaxial fixation using plate and screw method: A report of 160 treated patients. Neurosurgery 2002;51: 1351 -1357.

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Christian M. Puttlitz, Robert P. Melcher, Frank S. Kleinstueck, Juergen Harms, David S. Bradford, Jeffrey C. Lotz; Stability Analysis of Craniovertebral Junction Fixation Techniques. The Journal of Bone & Joint Surgery. 2004 Mar;86(3):561-568.

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