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AZADEH FARIN, M.D.,3 JENNI M. BUCKLEY, PH.D.,1,2 VEDAT DEVIREN, M.D.,1,2. R. TRIGG MCCLELLAN, M.D.,1,2 AND CHRISTOPHER P. AMES, M.D.1,3.
J Neurosurg Spine 12:517–524, 2010

Optimal reconstruction technique after C-2 corpectomy and spondylectomy: a biomechanical analysis Laboratory investigation Justin K. Scheer, B.S.,1,2 Jessica Tang, B.S.,1,2 Johnny Eguizabal, B.S.,1,2 Azadeh Farin, M.D., 3 Jenni M. Buckley, Ph.D.,1,2 Vedat Deviren, M.D.,1,2 R. Trigg McClellan, M.D.,1,2 and Christopher P. Ames, M.D.1,3 1 Biomechanical Testing Facility, Orthopaedic Trauma Institute, San Francisco General Hospital; and Departments of 2Orthopaedic Surgery and 3Neurological Surgery, University of California, San Francisco, California

Object. Primary spine tumors frequently involve the C-2 vertebra. Complete resection of the lesion may require total removal of the C-2 vertebral body, pedicles, and dens process. Authors of this biomechanical study are the first to evaluate a comprehensive set of reconstruction methods after C-2 resection to determine the optimal configuration depending on the degree of excision required. Methods. Eight human heads (from the skull to C-6) from 4 males and 4 females with a mean age of 68 ± 18 years at death were cleaned of tissue, while leaving ligaments and discs intact. Nondestructive flexion and extension (FE), lateral bending (LB), and axial rotation (AR) tests were conducted using a nonconstraining, pure moment loading apparatus, and relative motion across the fusion site (C1–3) was measured using a 3D motion tracking system. Specimens were tested up to 1.5 Nm at 0.25-Nm intervals for 45 seconds each. The spines were instrumented using 3.5-mm titanium rods with a midline occipitocervical plate (4.0 × 12–mm screws) and lateral mass screws (excluding C-2) at the C-1 (3.0 × 40 mm) and C3–5 levels (3.0 × 16 mm). Testing was repeated for the following configurations: Configuration 1 (CF1), instrumentation only from occiput to C-5; CF2, C-2 corpectomy leaving the dens; CF3, titanium mesh cage (16-mm diameter) from C-3 to C-1 ring and dens; CF4, removal of cage, C-1 ring, and dens; CF5, titanium mesh cage from C-3 to clivus (16-mm diameter); CF6, removal of C-2 posterior elements leaving the C3– clivus cage (spondylectomy); CF7, titanium mesh cage from C-3 to clivus (16-mm diameter) with 2 titanium mesh cages from C-3 to C-1 lateral masses (12-mm diameter); and CF8, removal of all 3 cages. A crosslink was added connecting the posterior rods for CF1, CF6, and CF8. Range-of-motion (ROM) differences between all groups were compared via repeated-measures ANOVA with paired comparisons using the Student t-test with a Tukey post hoc adjustment. A p < 0.05 indicated significance. Results. The addition of a central cage significantly increased FE rigidity compared with posterior instrumentation alone but had less of an effect in AR and LB. The addition of lateral cages did not significantly improve rigidity in any bending direction (CF6 vs CF7, p > 0.05). With posterior instrumentation alone (CF1 and CF2), C-2 corpectomy reduced bending rigidity in only the FE direction (p < 0.05). The removal of C-2 posterior elements in the presence of a C3–clivus cage did not affect the ROM in any bending mode (CF5 vs CF6, p > 0.05). A crosslink addition in CF1, CF6, and CF8 did not significantly affect primary or off-axis ROM (p > 0.05). Conclusions. Study results indicated that posterior instrumentation alone with 3.5-mm rods is insufficient for stability restoration after a C-2 corpectomy. Either C3–1 or C3–clivus cages can correct instability introduced by C-2 removal in the presence of posterior instrumentation. The addition of lateral cages to a C3–clivus fusion construct may be unnecessary since it does not significantly improve rigidity in any direction. (DOI: 10.3171/2009.11.SPINE09480)

Key Words      •      spine biomechanics      •      fusion      •      interbody cage      •      spondylectomy      •      en bloc resection      •      occipital cervical fusion

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upper cervical spine is a relatively common location for primary bone tumors and metastatic disease. Posterior fixation combined with adjuvant

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Abbreviations used in this paper: CF = configuration; ROM = range of motion.

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radiation23 in the setting of metastatic involvement and pathological fracture of C-2 can be clinically effective4 without resection; however, primary bone tumors have been shown to be best treated by en bloc resection.5,17,21,24 Since the first published report of cervical chordoma in 1959,19 en bloc resections of upper cervical chordomas 517

J. K. Scheer et al. have been described several times.1,7,10,13,16,18 The technique of en bloc resection has been shown to result in superior long-term local disease control for primary bone tumors.5,6,12 Whether en bloc3,13 or piecemeal15 resection is performed, most surgeons would advocate the radical excision14 of upper cervical chordomas. This strategy frequently involves complete removal of C-2, the odontoid process, C-2 posterior elements, and portions of the C-1 ring for access, which leaves an extremely unstable construct. Although the biomechanical effects of and reconstruction techniques for C-2 odontoid process resection have been well characterized, 20 the destabilizing effects of partial or complete resection of the C-2 body and a C-2 spondylectomy as well as the possible reconstruction strategies following a C-2 resection need further evaluation. While posterior hardware alone has long been the standard procedure to correct spinal instability,4 there is some concern that metallic devices placed in the anterior column after a C-2 corpectomy or spondylectomy may contribute to posterior pharyngeal erosion after radiation treatment, a complication occasionally observed in practice. While previous research22 has suggested the placement of lateral cages in addition to a central cage as a possible C-2 reconstruction technique following tumor resection, the proximity of the spinal cord, brainstem, and carotid and vertebral arteries adds a greater challenge and higher potential morbidity. The optimal surgical configuration required to both provide stability and reduce the risks of implementing such constructs remains unclear. Given the increased risk of adding anterior hardware to posterior fixation, the clinical relevance of finding an optimal balance between minimizing risk and maintaining stability must be addressed. Currently, a wide range of instrumentation is available to accommodate variable spinal anatomy following tumor resection. Extensive testing of surgical constructs comparing the efficacy of novel combinations of these implants would better characterize their ability to stabilize the spine. In particular, investigation into the various combinations of anterior hardware, including lateral mass cages, may provide valuable insight into the design best suited for certain procedures following the removal of tumors in different locations on the cervical spine. Furthermore, the extent to which crosslinks may restore lateral and torsional stability has not been studied in this model. The goal of our study was to determine the optimal instrumentation configuration following C-2 corpectomy that maximizes segmental rigidity while minimizing risk to the patient. Specifically, variables considered in this study include 1) the additional rigidity provided by anterior cages following C-2 corpectomy and odontoid/C-1 ring removal; 2) the necessity of lateral mass cages in addition to a central cage; and 3) the torsional and lateral bending stability provided by crosslinks. Biomechanical testing was performed on cadaveric head-neck specimens using a repeated-measures design, with each specimen subjected to 8 different surgical configurations. Outcome measures from this study included primary (on-axis) and secondary (off-axis) ROM in each of the 6 anatomical 518

bending directions. With its 8 different surgical configurations examined, this study is the first to encompass a broad range of fusion constructs to assess the optimal treatment post–tumor resection.

Methods Specimen Preparation

Eight fresh-frozen human heads (from the skull to C-6) from 4 males and 4 females with a mean age of 68 ± 18 years at the time of death were studied. Anteriorposterior and lateral radiographs of each specimen were obtained prior to full dissection to confirm normal anatomy and the absence of metastatic tumors. Dual energy x-ray absorptiometry (DEXA) scans were taken of each specimen with the C3–6 region mapped as L1–4 on the scanner’s internal software. These data provided a relative measurement of bone mineral density within the sample population, but they could not be used to determine the clinical degree of osteoporosis since the cervical spine is not a standard bone mineral density assessment site. Following radiographic assessment, the head-neck specimens were cleaned of muscles and connective tissue, taking care not to disrupt ligaments and intervertebral discs. The skull was transected at midcranium, inverted, and potted in a large metal tray using a quick-set resin (Smooth-Cast 300, Smooth-On). Similarly, the C-6 vertebra below the fusion site was potted to full depth in a small metal cup by using the quick-set resin.

Multidirectional Bending Tests

Multidirectional bending tests were conducted for each condition using a cable-driven pure moment testing apparatus8,11 mounted to a uniaxial hydraulic press (858 MiniBionix, MTS). Briefly, this system functions by inducing a pure moment (or force couple) at the top of the specimen via a circular loading ring. A single cable is wound around the ring, and tensioning this cable applies the force couple. Tension levels are controlled via the throw of the uniaxial hydraulic actuator, and applied moment is calculated as a function of the loading ring size and the cable tension as measured by the uniaxial load cell mounted to the hydraulic actuator. The cable can be wound in different directions on the loading ring to induce flexion and extension, right and left lateral bending, and right and left axial rotation of the entire spinal segment. To ensure that pure moment loading conditions were induced throughout each test, our validated 3D sliding ring set-up11 was used consisting of an x-y and rotary bearing at the base of the test frame and a counter-balanced loading ring on vertical bearings. Preliminary testing using this system for head-neck complexes showed that the weight of the head induces a bending artifact when positioned anatomically on the test frame; for this reason, the test specimens were inverted from anatomical position, with the head mounted to the base of the test frame and the caudal vertebra closest to the actuator (Fig. 1). During the bending tests, relative motion across the fusion site (C1–3) was measured using 3D motion tracking (Optotrak 3020, Northern Digital). Rigid body markJ Neurosurg: Spine / Volume 12 / May 2010

Optimal reconstruction after C-2 corpectomy and spondylectomy

Fig. 1.  Multidirectional bending tests were conducted on the cadaveric head-neck specimens using a cable-driven pure moment test set-up.  Left: View of the entire test set-up.  Right: Close-up of the loading ring component of the 3D sliding ring apparatus design.

ers (each consisting of 3 individual infrared sensors) were rigidly attached to the C-1 and C-3 vertebrae via cervical pedicle screws (3.5 × 16 mm, Depuy) placed anteriorly in the vertebral body. These screws were positioned so as not to interfere with reconstruction hardware, and this positioning was confirmed after each surgery by using planar radiography (BV Pulsera, Philips). Relative motion of the vertebrae in flexion and extension, lateral bending, and axial rotation bending directions was tracked in real time from the 3D camera system using custom-designed software (FlexWin 2008, Barrow Neurological Institute). This hardware and software system has a validated accuracy of 0.1 degree for spinal testing.9 Nondestructive flexion and extension, lateral bending, and axial rotation tests were performed on each specimen in accordance with a standard protocol.8 Specifically, for each loading direction, specimens were subjected to 3 cycles from 0 to 1.5 Nm in 0.25-Nm increments (45-second hold at each increment), and data were recorded on the final cycle. Fusion Configurations Following C-2 Corpectomy

Each spine was fixated using lateral mass screws (excluding C-2) at the C-1 (3.0 × 40 mm) and C3–5 levels (3.0 × 16 mm) and a midline occipitocervical plate with standard 3.5-mm titanium rods contoured to fit with rod benders. Testing was repeated for the following cervical configurations (Fig. 2): CF1, instrumentation from the oc-

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ciput to C-5; CF2, C-2 corpectomy removing the posterior longitudinal ligament and leaving the odontoid; CF3, titanium mesh cage screw fixated from C-3 to the ring of C-1 and the odontoid (16 mm in diameter); CF4, removal of the cage, C-1 anterior ring, and the odontoid; CF5, titanium mesh cage screw fixated from C-3 to the clivus (16 mm in diameter); CF6, removal of the posterior elements of C-2 while leaving the cage from C-3 to the clivus (that is, complete C-2 spondylectomy); CF7, titanium mesh cage from C-3 to the clivus (16 mm in diameter) along with 2 titanium mesh cages from the lateral masses of C-3 to the lateral masses of C-1 (12 mm in diameter); and CF8, posterior instrumentation alone from the occiput to C-5 for a complete C-2 spondylectomy. In addition to the 8 configurations above, a crosslink connecting the C-1 lateral mass screws was added to CF1, CF6, and CF8 for 4 of the 8 specimens to test its effectiveness in increasing rigidity. Constructs with and without crosslinks were compared by combining measurements from the C0–1 level and C1–3 level to determine the overall primary ROM across the fusion site from C-0 to C-3. A crosslink addition to the C3–clivus cage without C-2 was compared with the configuration consisting of only the C3–clivus cage with 2 lateral cages (CF6 vs CF7) to determine whether a crosslink could act as a substitute for the 2 lateral cages. Outcome Measures

Repeated-measures ANOVA with paired compari519

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Fig. 2.  Fusion configurations following C-2 corpectomy. Configurations 1 through 8 are represented in each of the panels (A–H, respectively).

sons was made using the Student t-test with a Tukey post hoc adjustment (JMP, versions 5.0, SAS Institute, Inc.) to analyze differences in the primary ROM (motion in the loading direction) across all constructs. Off-axis ROM was compared for a subset of structures—namely, CF6, CF7, and CF8—each with and without crosslinks. Offaxis motion takes into account the 2 other directions of motion that are not being tested; for example, off-axis motion for flexion and extension tests includes axial rotation and lateral bending motion. The absence of a significant difference between off-axis motion confirms that no artifact exists to mislead the interpretation of data. The level of significance for all statistical tests was set at p < 0.05.

Results

Significant differences in the primary and off-axis ROM between the different fusion configurations are graphically presented in Figs. 3–6. Results are summarized below for each of the 4 clinical issues of interest. Anterior Hardware Addition Following C-2 Corpectomy and Odontoid/C-1 Ring Removal

For posterior-only constructs, a C-2 corpectomy significantly increased the ROM in flexion and extension compared with an intact anterior column (CF2 vs CF1, p < 0.01). Subsequent removal of the odontoid/C-1 ring

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did not further increase the ROM in any anatomical direction (CF4 vs CF2, p > 0.05). Placement of a C3–clivus cage reversed this instability completely in flexion and extension and axial rotation. For cases with a C-2 corpectomy, placement of a C1–3 cage anteriorly reversed instability in flexion and extension. With this cage in place, the additional removal of C-2 posterior elements (simulating complete C-2 spondylectomy) did not result in further instability in any direction (CF5 vs CF6, p > 0.05 for all modes). Addition of Lateral Mass Cages to Central Cages

The addition of 2 lateral cages did not significantly change primary or off-axis ROM in any bending direction (all comparisons CF6 vs CF7, p > 0.05).

Addition of Crosslink

Crosslink addition to the posterior rods of CF1, CF6, and CF8 did not significantly affect primary or off-axis ROM.

Discussion

The results of this study indicate that the mechanical stability of cervical fusion constructs following C-2 corpectomy is dependent on instrumentation configuration and the extent of C-1 and C-2 resection. Removal of the C-2 body in the presence of posterior instrumentation J Neurosurg: Spine / Volume 12 / May 2010

Optimal reconstruction after C-2 corpectomy and spondylectomy

Fig. 3.  Bar graph showing primary ROM for flexion and extension for all specimens. Error bars denote ± 1 SD. corp = corpectomy; OCC = occiput.

(occiput–C5) destabilized the construct in flexion and extension, and this instability was not increased by further removal of the odontoid/C-1 ring. Instability was completely corrected by the addition of a single anterior cage, either spanning from C-3 to the clivus or from C-3 to the odontoid/C-1 ring. In the presence of a C3–clivus cage, the degree of resection at C-2—that is, corpectomy versus spondylectomy—had no mechanical effect. Furthermore,

the addition of lateral mass cages to the fusion construct did not improve rigidity in any bending direction, although it did provide a greater surface area for fusion. Similarly, crosslinks joining the posterior rods at C-1 also contributed no structural effect. Currently, 3.5-mm posterior rod fixation systems are inadequate to prevent instability after C-2 corpectomy or spondylectomy. This instability is completely corrected

Fig. 4.  Bar graph demonstrating primary ROM for axial rotation for all specimens. Error bars denote ± 1 SD.

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Fig. 5.  Bar graph revealing the primary ROM for lateral bending for all specimens. Error bars denote ± 1 SD.

by the fixation of anterior cages screwed to the remaining osseous structures. Despite the potential increase in complications, results demonstrated that anterior load-bearing devices are required after C-2 resection to prevent instability. To our knowledge, no biomechanical studies to date have addressed the issue of whether long posterior fixation alone, including the occiput, could result in sufficient stability to obviate the often difficult placement of an anterior load-bearing device at C-2 following C-2 corpectomy or spondylectomy. In addition, prior to this study, the stability of varying degrees of C-2 resection with posterior fixation had not been quantified or compared. Although Suchomel et al.22 have proposed a 3-column reconstruction of the cervical spine following C-2 spondylectomy, the results of our study suggest the futility of this approach given its inability to significantly increase rigidity while remaining a high-risk procedure. Rather, posterior fixation used in conjunction with a single anterior cage presents the most favorable design to balance increased stability with minimal risk to patients following tumor removal. This study has several strengths. First, it is a comprehensive analysis of 8 different surgical configurations with 504 tests conducted in total. The experimental design allowed examination of micromotion across the fusion site under physiological multiaxial bending conditions to an accuracy of 0.1°. Both primary and off-axis motions were considered to determine both inconsistent data interpretation and the propensity of micromotion to result in nonunions. Moreover, the repeated-measures test design used for data analysis controls for donor effects. As the first study to test many surgical configurations at once, we recommend an optimal construct to maximize stability and minimize risks to patients based on extensive research. 522

This study embodies a few limitations. It was not logistically possible to randomize treatment order, and consequently the randomized specimens probably became more flexible during later tests because of repeated testing. However, the order of treatment—that is, the order in which the specimens were instrumented with the different surgical configurations—introduces increasingly stable constructs. This trend runs counter to the tendency of specimens to exhibit increased flexibility during later tests. Therefore, outcomes due to this limitation should not severely restrict the interpretations of our study data. Moreover, because only postoperative conditions were taken into account, performing additional fatigue testing to simulate physiological conditions would largely improve this study. Further fatigue tests would allow the assessment of possible failure mechanisms within these constructs. Crosslinks were introduced later in the study so that positioning of a crosslink could not be optimized. Specifically, the design of the top-mounted crosslinks used required them to be added at a screw-fixated level (C-1) near the edge of the fusion site. Authors of future studies may look at placing the crosslink at the C-2 level. They may also look at larger diameter rods and CoCr alloys in this model to determine whether posterior fixation alone with stiffer rods can decrease the clinical necessity of placing anterior implants in the posterior pharynx.

Conclusions

Primary tumors located in the upper cervical spine continue to necessitate surgical intervention to prevent neurological compromise, achieve local disease control, and create or maintain regional stability.2,5 Nonetheless, complete tumor removal and reconstruction in this area remains a significant challenge. Our comprehensive overJ Neurosurg: Spine / Volume 12 / May 2010

Optimal reconstruction after C-2 corpectomy and spondylectomy Buckley. Drafting the article: JK Scheer, JA Tang, A Farin, JM Buckley, V Deviren, RT McClellan, C Ames. Critically revising the article: JK Scheer, JA Tang, A Farin, JM Buckley, V Deviren, RT McClellan, C Ames. Reviewed final version of the manuscript and approved it for submission: JK Scheer, JM Buckley, V Deviren, RT McClellan, C Ames. Statistical analysis: JK Scheer, JA Tang, JM Buckley. Administrative/technical/material support: JK Scheer, JM Buckley, RT McClellan, C Ames. Study supervision: JK Scheer, JM Buckley. References

Fig. 6.  Statistically significant differences between groups. Groups not connected by a shaded column are statistically different. p < 0.05 for pairwise analysis using paired t-tests with Tukey adjustment.

view of various surgical configurations reveals an optimal configuration: posterior fixation along with a single anterior cage extending across the fusion site offers the most stability. Further removal of the odontoid/C-1 ring does not result in significantly more instability than removal of the C-2 body. If tumor resection requires C-2 corpectomy, posterior fixation along with a cage extending from C-3 to the odontoid is sufficient to maintain stability. If further removal of the odontoid and C-1 anterior ring is required, then posterior fixation along with a C3–clivus cage is sufficient to maintain stability. The additional removal of C-2 posterior elements for complete spondylectomy does not result in increased instability when an anterior cage is used. Disclosure Funding was provided by Depuy Spine (J.M.B.). Drs. Deviren, McClellan, and Ames are consultants for Stryker; Acumed and Spinal Kinetics; and Stryker, respectively. Conception and design: J Eguizabal, JM Buckley, V Deviren, C Ames. Acquisition of data: JK Scheer, JA Tang, J Eguizabal. Analysis and interpretation of data: JK Scheer, JA Tang, JM

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24.  Tomita K, Tsuchiya H: Total sacrectomy and reconstruction for huge sacral tumors. Spine 15:1223–1227, 1990 Manuscript submitted June 2, 2009. Accepted November 16, 2009. Portions of this work were presented in poster form at the Orthopaedic Research Society Conference held in Las Vegas, Nevada, February 21–25, 2009; the 2009 Summer Bioengineering Conference, American Society of Mechanical Engineers held in Lake Tahoe, California, June 17–21, 2009; and the International Meeting on Advanced Spine Techniques, Scoliosis Research Society, held in Vienna, Austria, July 15–18, 2009. Address correspondence to: Justin K. Scheer, B.S., Biomechanical Testing Facility, San Francisco General Hospital, 1001 Potrero Avenue, Building 100, Room 123, San Francisco, California 94110. email: [email protected].

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