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Biomechanical Study of Novel Unilateral Fixation Combining Unilateral Pedicle and Contralateral Translaminar Screws in the Subaxial Cervical Spine
Original Article
Biomechanical Study of Novel Unilateral Fixation Combining Unilateral Pedicle and Contralateral Translaminar Screws in the Subaxial Cervical Spine Lei Shi, Kai Shen, Lei Chu, Ke-Xiao Yu, Qing-Shuai Yu, Rui Deng, Zhong-Liang Deng
INTRODUCTION: In several situations, the stability of the subaxial cervical spine is damaged and involves the lateral mass of 1 side; in these cases, a pedicle screw (PS) or lateral mass screw (LMS) may not be suitable for placement on the affected side. Therefore, salvage shortsegment fixation with satisfactory stability is needed when bilateral fixation is not feasible.
biomechanical tests and may play a clinical role when BPS or BMS placement is not feasible for short-segment fixation.
METHODS: Seven fresh-frozen human cervical spine specimens were used to test the 3-plane range of motion (ROM) of the C4-C5 segment. Quasistatic 2-Nm flexibility testing was performed in the following sequence: 1) intact; 2) destabilization (using 3-column injury models) treated with bilateral mass screws (BMSs); 3) destabilization treated with a unilateral PS combined with a contralateral translaminar screw (UPSDCTLS); and 4) destabilization treated with bilateral PSs (BPSs). Then, a pullout strength test was performed for the PSs, LMSs, and translaminar screws (TLSs) using 7 isolated C4 and C5 vertebrae.
INTRODUCTION
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RESULTS: The UPSDCTLS group showed no significant difference from the BMS group in the 3-plane ROM or from the BPS group in the axial rotation or flexion-extension ROM but showed a significantly greater lateral bending ROM than did the BPS group. The pullout strength test showed that both C4 and C5 TLSs had strength similar to that of LMSs but poorer than that of PSs.
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CONCLUSIONS: Fixation with the hybrid UPSDCTLS construct performed as well as BMS fixation in our
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Key words Biomechanical study - Pullout strength - Range of motion - Subaxial cervical spine - Translaminar screw - Unilateral fixation -
Abbreviations and Acronyms BMS: Bilateral mass screw BPS: Bilateral pedicle screw LMS: Lateral mass screw LT: Laminar thickness PS: Pedicle screw ROM: Range of motion TLS: Translaminar screw
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osterior cervical screw-rod fixation is performed using pedicle screw (PS) or lateral mass screw (LMS) techniques, both of which are common for stabilization of the cervical spine.1-4 However, in several situations, such as the occurrence of tumors, fractures, or tuberculosis, the stability of the cervical spine is damaged and involves the lateral mass on 1 side; in such cases, PS or LMS placement may not be suitable on the affected side. Moreover, unilateral short-segment fixation cannot achieve sufficient biomechanical stability, and multisegment fixation over the affected level sacrifices the motion of the adjacent segment.5-7 Therefore, salvage short-segment fixation with satisfactory stability is needed when bilateral fixation is not feasible in the subaxial cervical spine. Translaminar screws (TLSs) were initially used to avoid injury to the vertebral artery (VA) that might occur during transarticular or PS fixation.8 The safety and efficacy of TLSs in C2 have been shown.9-12 Therefore, TLS placement has gained popularity as an alternative salvage technique and has been applied to the subaxial cervical and thoracic spine.13-18 Shen et al.9 proposed a novel approach consisting of unilateral C1 posterior arch screw and C2 laminar screw placement combined with an ipsilateral crossed C1-C2 PS-rod fixation technique for treating atlantoaxial
UPSDCTLS: Unilateral pedicle screw combined with contralateral translaminar screw VA: Vertebral artery Department of Orthopedics, the Second Affiliated Hospital of Chongqing Medical University, Chongqing, PR China To whom correspondence should be addressed: Zhong-Liang Deng, M.D., Ph.D. [E-mail: [email protected]; [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.09.191 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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Figure 1. Laminar screw insertion trajectory. (A) indicates the entry point, and the white arrows indicate the laminar outline under oblique fluoroscopy (axial view of lamina). (B) Cylinder simulating the translaminar screw; the tip of the screw should not
instability; this construct showed satisfactory biomechanical properties and prompted us to investigate whether we could apply hybrid unilateral fixation in the subaxial cervical spine. Because C4 and C5 have the narrowest lamina, they also have the lowest acceptance rates of 3.5-mm TLSs in the subaxial cervical spine.19-21 Therefore, we chose the C4-C5 segment as a representative segment for investigating the biomechanical properties of a novel unilateral hybrid fixation method consisting of a unilateral PS combined with a contralateral TLS (UPSþCTLS) compared with
pass the medial margin of the lateral mass (white dotted line), and the screw orientation should be parallel to the slope of the lamina under anteroposterior fluoroscopy.
traditional fixation using bilateral mass screws (BMSs) and bilateral PSs (BPSs) in cadaveric subaxial cervical spine models. METHODS Specimen Preparation After obtaining approval from the medical ethics committee of the institutional review board, 7 fresh-frozen human cadaveric cervical spine specimens (C0-C7) were obtained from 3 male and 4 female
Figure 2. Stabilization by different fixation techniques at the C4-C5 segment. (A) Bilateral mass screws. (B) Unilateral pedicle screw combined with a contralateral laminar screw. (C) Bilateral pedicle screws.
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donated cadavers and used in this biomechanical study. The mean age of the cadavers was 67 years (range, 51e78 years). Spiral computed tomography scans of each specimen (C4-C5) were obtained, and three-dimensional images were analyzed to exclude fractures and obvious degeneration or deformities. The laminar thickness (LT) of C4 and C5 was measured as the minimum thickness spanning from the ventromedial to the dorsolateral side at the central portion of the lamina bilaterally. Hence, specimens were excluded if the LT on 1 side was <3.5 mm as determined by image-based measurements. Specimens were wrapped in salinemoistened gauze, double-bagged in plastic, and frozen at e20 C. Before testing, the specimens were thawed at room temperature, and all musculature was carefully removed and all ligaments, discs, and facet joint capsules were completely preserved. Thereafter, the C0 (cranial occipital bone) and C7 vertebrae were embedded in a custom-made metal mold containing polymethylmethacrylate bone cement such that C4 was aligned horizontally. The specimens were sprayed with saline to keep them moist throughout the experiment. Biomechanical Experiments A flexibility test was first performed on all intact specimens, followed by the 3-column destabilization procedure consisting of incising the anterior longitudinal ligament, supraspinous and interspinous ligaments, facet capsules, ligamentum flavum, and posterior longitudinal ligament and completely transecting the annulus fibrosis and nucleus pulposus at C4-C5.3,16 After 3-column injury and dorsal stabilization, all 7 specimens were tested in order with BMS, UPSþCTLS, and BPS fixation. After UPSþCTLS testing, the UPS was left in place for BPS testing. Specimen Instrumentation Instrumentation applied with the implant (PCF [Wego Co., Weihai, Shandong, China]) included a titanium alloy system consisting of 3.2-mm rods and self-tapping multiaxial screws with an outer diameter of 3.5 mm. To achieve reliable screw positioning, screw insertion was performed under C-arm fluoroscopy. For PS placement, we first used landmarks to locate the entry points of the pedicle22 and then used a high-speed drill to open the entry cortex. The standard process for pedicle insertion was then performed. The optimal screw length close to the anterior cortex of the vertebral body was determined in the preoperative planning of the screw trajectories. The screws were 26e32 mm long. For LMS placement, we used the technique described by Magerl.2,3 The screw length was chosen to achieve bicortical fixation with 2 screw threads penetrating the anterior cortex. Before screw insertion, the correct drilling position was verified by manual palpation with a dissector, followed by the insertion of 3. 5-mm-diameter screws. The screws were 12e16 mm long. For TLS placement, the screw entry point was located at the initiation of the lamina from the spinous process at the midpoint of its dorsal arch. A high-speed drill was used to open the entry cortical window. Using a thin pedicle finder, the contralateral lamina was carefully drilled along its length, with the pedicle finder aimed at the lateral mass. Procedures were performed under oblique cervical fluoroscopy (axial view of the lamina) to confirm that the pedicle finder did not violate the inner cortex of
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Figure 3. Pullout strength test. Vertebral bodies were embedded individually in polymethylmethacrylate cement. The pullout test was performed along the axis of the screw at a loading rate of 2 mm/minute.
the lamina. Typically, the tip of the screw should not pass the medial margin of the lateral mass, and its orientation should be parallel to the slope of the lamina under anterior-posterior fluoroscopy13,14,23 (Figure 1). The screws were 18e22 mm long. For the experimental protocol, the screws were inserted into each vertebra from C4 to C5, followed by attachment of the rods (Figure 2).
Flexibility Test The range of motion (ROM) was tested with the MTS 858 Mini Bionix II test system (MTS Systems Corp., Eden Prairie, Minnesota, USA). The specimens were loaded using a testing system of cables and pulleys that applied pure moments and induced 3-plane movement, including flexion-extension, lateral bending, and axial rotation. Each movement was used in 3 loadingunloading cycles to a maximum torque of 2 Nm at a rate of 0.1 Nm/second. The loading was held constant for 10 seconds to minimize the viscoelastic effect. Two preconditioning cycles were performed, and data were recorded during the third loading cycle.24 During these tests, the relative motion between C4 and C5 was measured using a three-dimensional spine motion
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Table 1. The Range of Motion ( ) at the C4-C5 During Different Fixation Statuses Bilateral Mass Screw
Unilateral Pedicle Screw Combined with a Contralateral Laminar Screw
Testing Modes
Intact
Bilateral Pedicle Screw
Flexion-extension
16.12 8.73
15.576.93
13.783.47
11.795.69
Lateral bending
12.76 4.00
6.6 5.71*
7.55 2.92*
2.21 0.90*yz
Axial rotation
9.98 3.79
2.49 1.18*
2.22 0.99*
1.36 0.45*
*A significant difference from the intact (P < 0.05). yA significant difference from the bilateral mass screw (P < 0.05). zA significant difference from the unilateral pedicle screw combined with a contralateral laminar screw (P < 0.05).
measurement system (6 Eagle System [Motion Analysis Co., Woburn, Massachusetts, USA]) to process images to identify, locate, and calculate markers of the C4 and C5 positions in space.
Pullout Strength Test After the flexibility test, all C4 and C5 vertebrae were isolated by stripping the remaining soft tissue, and the vertebral bodies were embedded individually in custom-made molds with polymethylmethacrylate cement. The vertebrae were then fixed in the materials testing instrument (Material Testing System Inc., Minneapolis, Minnesota, USA) with their PS, LMS, or TLS attached to a custom clamp (Figure 3). To reduce mutual interference, the PS and TLS were tested on one side of each vertebra, and the LMS was tested on the other side. The maximum displacement and pullout strength were set to 10 mm and 3000 N, respectively. The screw pullout test was performed along the axis of the screw at a loading rate of 2 mm/minute until an abrupt change in the curved slope of the loading displacement was noted. The axial pullout force was defined as the peak load-to-failure.25
Figure 4. The primary stability of the different fixation techniques is represented by the average ROM in 3 loading planes (flexion/extension, lateral bending, and axial rotation). * Significant difference (P < 0.05). BMS,
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Statistical Analysis In the statistical analysis, analysis of variance with the StudentNewman-Keuls post hoc test (P < 0.05) was used to examine differences among the groups. Analyses were performed with SPSS Statistics for Windows, version 19.0 (IBM Corp., Armonk, New York, USA).
RESULTS No significant differences were observed in the flexion-extension ROM among the groups. However, the 3 fixation groups showed significantly lower ROMs than did the intact group in lateral bending and axial rotation. The UPSþCTLS group showed no significant difference from the BMS group in the 3-plane ROM. However, the UPSþCTLS and BMS groups showed significantly greater lateral bending than the BPS group. All data are presented in Table 1 and Figure 4. The pullout strength test showed that the average pullout strength values of C4 with a PS, LMS, and TLS were 553 177 N, 264 120 N and 311 152 N, respectively. The PS strength was greater than that of the LMS (P ¼ 0.002) and TLS (P ¼ 0.008). The
bilateral mass screw; BPS, bilateral pedicle screw UPSþCTLS, unilateral pedicle screw combined with a contralateral laminar screw.
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Table 2. Axial Pullout Strength Pedicle Screw
Lateral Mass Screw
Translaminar Screw
C4 pullout load (N)
553 177
264 120*
311 152*
C5 pullout load (N)
585 118
247 94*
349 208*
*A significant difference from the pedicle screw (P < 0.05).
TLS strength was slightly greater but not significantly different from the LMS strength. Similar results were observed for pullout strength in C5 (Table 2).
DISCUSSION In several situations, such as the occurrence of tumors, fractures, or tuberculosis, the stability of the cervical spine can be damaged and involve the lateral mass of 1 side; in such cases, PS or LMS placement may not be suitable on the affected side. However, unilateral short-segment fixation cannot achieve sufficient biomechanical stability, and multisegment fixation over the affected level sacrifices the motion of the adjacent segment.5-7 Therefore, salvage short-segment fixation with satisfactory stability is needed when bilateral fixation is not feasible in the subaxial cervical spine. Unilateral fixation is generally used to prevent VA injury when asymmetry or unilateral occlusion is present.26 One study has shown that the incidence of VA occlusion induced by traumatic cervical spine injury is as high as 17.2%.27 Moreover, VA injury has been directly linked to intraoperative or perioperative death when the VA communicates only unilaterally with the basilar artery or has an obviously dominant side. In this situation, even proficient surgeons cannot guarantee 100% accuracy in PS or LMS placement without slight violation of the VA, although the rates of injury are low.28,29 Therefore, the TLS technique, as it was initially designed, is the safest for avoiding violation of the VA. The TLS technique is used to avoid injury to the VA that might occur during transarticular or PS fixation in C2 and was first described by Neill Wright in 2004.4 The TLS technique gained popularity as an alternative salvage technique and was then expanded to the subaxial cervical and thoracic spine.13-18 Shen et al.9 proposed a novel approach consisting of unilateral C1 posterior arch screw and C2 laminar screw placement combined with an ipsilateral crossed C1-C2 PS-rod fixation technique for treating atlantoaxial instability. The technique used 1-sided fixation, and the construct showed satisfactory biomechanical properties equal to those of BPSs. This development prompted us to investigate whether we could apply hybrid unilateral fixation to the subaxial cervical spine as an alternative salvage technique when bilateral fixation is not feasible. To the best of our knowledge, no previous studies using a hybrid technique in the subaxial cervical spine have been reported in the literature. Before the clinical application of this technique, biomechanical studies should be performed to examine the resulting biomechanical properties and show the feasibility of the technique. Furthermore, bilateral
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Figure 5. Notching technique. Place the screw through the basilar part of the spinosus process to the lamina, notch the outside of the lamina, and place the screw within the notch into the lateral mass.
fixation requires dissection of the posterior cervical musculature, resulting in increased invasiveness. In contrast, unilateral fixation reduces the disruption of the soft tissue, potentially reducing postoperative muscular dysfunction, pain, and disability.30 The use of LMSs is more popular than that of PSs in the subaxial cervical spine because of the superior safety and efficacy. However, the effective length of LMSs is shorter than that of PSs. This drawback resulted in unsatisfactory biomechanical stability in 3-column destabilization cervical models in the preliminary experiment. This is the main reason why we did not choose to use a construct of LMSs and TLSs. In addition, PS and TLS placement can be observed by oblique fluoroscopy; the screws are parallel to each other, and the rod can be easily inserted and placed. The clinical application of TLSs in the subaxial cervical spine is limited because of the narrowness of the lamina. Alvin et al.19 found that C5 had the smallest LT in the subaxial spine, followed by C4, and C3-C5 showed lower mean unilateral translaminar 3.5-mm screw acceptance rates (<52%). Ji et al.21 found a higher likelihood of successful TLS placement in a Korean population than in an American population. Therefore, TLSs are of limited value as a salvage technique when used in clinical situations in which bilateral fixation is not suitable. However, how should cases in which the LT is <3.5 mm be addressed? It might be appropriate to use a smaller screw diameter or a notching technique to place the screw through the basilar part of the spinosus process to the lamina, notch the outside of the lamina, and place the screw within the notch into the lateral mass (Figure 5). In the ROM tests, we calculated the total values of both directions on 1 plane of movement to minimize error. The data showed no significant differences in the flexion-extension ROM among the groups. We speculate that the reason for this lack of
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difference was that the cervical spine has the largest flexionextension ROM and because 3-column injury cadaveric models are unstable, increasing the difficulty of achieving sufficient biomechanical stability with posterior fixation. Moreover, UPSþCTLS versus BMS fixation showed no significant differences in the 3-plane ROM or pullout strength, although the average values were greater for UPSþCTLS fixation. Therefore, we deemed that the UPSþCTLS construct has biomechanical properties similar to those of the BMS construct. Compared with BPS, UPSþCTLS showed no significant differences in the axial rotation or flexion-extension ROM but showed a significantly greater lateral bending ROM. These data indicate that it is difficult to achieve rigid stability comparable to that of BPS via 1-sided fixation with the UPSþCTLS construct. The TLS pullout strength was also significantly poorer than the PS pullout strength. Our study has validated the feasibility of the UPSþCTLS construct by biomechanical testing. However, this study has some limitations. First, the sample size was limited by the number of
REFERENCES 1. Kothe R, Ruther W, Schneider E, Linke B. Biomechanical analysis of transpedicular screw fixation in the subaxial cervical spine. Spine (Phila Pa 1976). 2004;29:1869-1875. 2. Xu R, McGirt MJ, Sutter EG, Sciubba DM, Wolinsky JP, Witham TF, et al. Biomechanical comparison between C-7 lateral mass and pedicle screws in subaxial cervical constructs. Presented at the 2009 Joint Spine Meeting. Laboratory investigation. J Neurosurg Spine. 2010;13:688-694. 3. Bozkus H, Ames CP, Chamberlain RH, Nottmeier EW, Sonntag VK, Papadopoulos SM, et al. Biomechanical analysis of rigid stabilization techniques for three-column injury in the lower cervical spine. Spine (Phila Pa 1976). 2005;30: 915-922. 4. Jones EL, Heller JG, Silcox DH, Hutton WC. Cervical pedicle screws versus lateral mass screws. Anatomic feasibility and biomechanical comparison. Spine (Phila Pa 1976). 1997;22:977-982. 5. Ando K, Imagama S, Ito Z, Kobayashi K, Ukai J, Muramoto A, et al. Unilateral instrumented fixation for cervical dumbbell tumors. J Orthop Surg Res. 2014;9:2. 6. Bhatia N, Rama A, Sievers B, Quigley R, McGarry MH, Lee YP, et al. Biomechanical Evaluation of unilateral versus bilateral C1 lateral mass-C2 intralaminar fixation. Global Spine J. 2017; 7:239-245. 7. Riesenburger RI, Potluri T, Kulkarni N, Lavelle W, Roguski M, Goel VK, et al. Unilateral cervical facet dislocation: a biomechanical study of several constructs including unilateral lateral mass fixation supplemented by an interspinous cable. J Neurosurg Spine. 2012;16:251-256. 8. Wright NM. Posterior C2 fixation using bilateral, crossing C2 laminar screws: case series and technical note. J Spinal Disord Tech. 2004;17: 158-162.
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cadaver donations, and some specimens with a narrow LT were excluded by computed tomography examinations before testing. The fixation fatigue test was not completed because of the small sample size. Therefore, we could not examine long-term stability. Second, the pullout strength test was performed after the ROM test, which may result in underestimation of the true pullout strength. It is difficult to translate the results of biomechanical studies of any type into general clinical conclusions. Although we acknowledge the highly unstable nature of this model, the data obtained from the biomechanical tests can be used a reference for clinical usage. CONCLUSIONS Fixation with the hybrid UPSþCTLS construct performed as well as BMS fixation in our biomechanical tests and may play a clinical role when BPS or BMS fixation is not feasible for short-segment fixation.
9. Shen K, Deng Z, Yang J, Liu C, Zhang R. Biomechanical study of novel unilateral C1 posterior arch screws and C2 laminar screws combined with an ipsilateral crossed C1-C2 pedicle screw-rod fixation for atlantoaxial instability. Arch Orthop Trauma Surg. 2017;137:1349-1355. 10. Guo-Xin J, Huan W. Unilateral C-1 posterior arch screws and C-2 laminar screws combined with a 1side C1-2 pedicle screw system as salvage fixation for atlantoaxial instability. J Neurosurg Spine. 2015: 1-6. 11. Du S, Ni B, Lu X, Xie N, Guo X, Guo Q, et al. Application of unilateral C2 translaminar screw in the treatment for atlantoaxial instability as an alternative or salvage of pedicle screw fixation. World Neurosurg. 2017;97:86-92. 12. Dorward IG, Wright NM. Seven years of experience with C2 translaminar screw fixation: clinical series and review of the literature. Neurosurgery. 2011;68:1491-1499 [discussion: 1499]. 13. Shin SI, Yeom JS, Kim HJ, Chang BS, Lee CK, Riew KD. The feasibility of laminar screw placement in the subaxial spine: analysis using 215 three-dimensional computed tomography scans and simulation software. Spine J. 2012;12:577-584. 14. Cho W, Le JT, Shimer AL, Werner BC, Glaser JA, Shen FH. Anatomy of lamina in the subaxial cervical spine with the special reference to translaminar screws: CT and cadaveric analysis with screw trajectory simulation. Clin Spine Surg. 2017; 30:E535-E539. 15. Cho W, Le JT, Shimer AL, Werner BC, Glaser JA, Shen FH. The insertion technique of translaminar screws in the thoracic spine: computed tomography and cadaveric validation. Spine J. 2015;15: 309-313. 16. Kretzer RM, Hu N, Kikkawa J, Garonzik IM, Jallo GI, Tortolani PJ, et al. Surgical management of two- versus three-column injuries of the cervicothoracic junction: biomechanical comparison of translaminar screw and pedicle screw fixation using a cadaveric model. Spine (Phila Pa 1976). 2010;35:E948-E954.
17. Hong JT, An H, Park C-K, Lee SW. Significance of laminar screw fixation in the subaxial cervical spine. Spine J. 2008;8:116S-117S. 18. Jea A, Johnson KK, Whitehead WE, Luerssen TG. Translaminar screw fixation in the subaxial pediatric cervical spine. J Neurosurg Pediatr. 2008;2: 386-390. 19. Alvin MD, Abdullah KG, Steinmetz MP, Lubelski D, Nowacki AS, Benzel EC, et al. Translaminar screw fixation in the subaxial cervical spine: quantitative laminar analysis and feasibility of unilateral and bilateral translaminar virtual screw placement. Spine (Phila Pa 1976). 2012; 37:E745-E751. 20. Yusof MI, Shamsi SS. Translaminar screw fixation of the cervical spine in Asian population: feasibility and safety consideration based on computerized tomographic measurements. Surg Radiol Anat. 2012;34:203-207. 21. Ji GY, Oh CH, Park SH, Kurniawan F, Lee J, Jeon JK, et al. Feasibility of translaminar screw placement in Korean population: morphometric analysis of cervical spine. Yonsei Med J. 2015;56: 159-166. 22. Karaikovic EE, Kunakornsawat S, Daubs MD, Madsen TW, Gaines RW Jr. Surgical anatomy of the cervical pedicles: landmarks for posterior cervical pedicle entrance localization. J Spinal Disord. 2000;13:63-72. 23. Jea A, Sheth RN, Vanni S, Green BA, Levi AD. Modification of Wright’s technique for placement of bilateral crossing C2 translaminar screws: technical note. Spine J. 2008;8:656-660. 24. Tong J, Ji W, Zhou R, Huang Z, Liu S, Zhu Q. Biomechanical comparison of transfacet screws to lateral mass screw-rod constructs in the lower cervical spine. Eur Spine J. 2015;25:1787-1793. 25. Klekamp JW, Ugbo JL, Heller JG, Hutton WC. Cervical transfacet versus lateral mass screws: a biomechanical comparison. J Spinal Disord. 2000; 13:515-518.
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26. Matsubara T, Mizutani J, Fukuoka M, Hatoh T, Kojima H, Otsuka T. Safe atlantoaxial fixation using a laminar screw (intralaminar screw) in a patient with unilateral occlusion of vertebral artery: case report. Spine (Phila Pa 1976). 2007;32: E30-E33.
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screws: a systematic review. J Neurosurg Spine. 2013; 19:614-623. 29. Guan Q, Chen L, Long Y, Xiang Z. Iatrogenic vertebral artery injury during anterior cervical spine surgery: a systematic review. World Neurosurg. 2017;106:715-722.
27. Taneichi H, Suda K, Kajino T, Kaneda K. Traumatically induced vertebral artery occlusion associated with cervical spine injuries: prospective study using magnetic resonance angiography. Spine (Phila Pa 1976). 2005;30:1955-1962.
30. Wang MY, Levi ADO. Minimally invasive lateral mass screw fixation in the cervical spine: initial clinical experience with long-term follow-up. Neurosurgery. 2006;58:907-912.
28. Yoshihara H, Passias PG, Errico TJ. Screw-related complications in the subaxial cervical spine with the use of lateral mass versus cervical pedicle
Conflict of interest statement: This study was supported by the Special Foundation for the Social Safeguard and
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Scientific Innovation of Chongqing (number cstc2016shmsztzx10001-6) and the Chongqing Research and Innovation Project of Graduate Students (number YB17112). Received 28 July 2018; accepted 25 September 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.09.191 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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Biomechanical Study of Novel Unilateral Fixation Combining Unilateral Pedicle and Contralateral Translaminar Screws in the Subaxial Cervical Spine Lei Shi, Kai Shen, Lei Chu, Ke-Xiao Yu, Qing-Shuai Yu, Rui Deng, Zhong-Liang Deng
INTRODUCTION: In several situations, the stability of the subaxial cervical spine is damaged and involves the lateral mass of 1 side; in these cases, a pedicle screw (PS) or lateral mass screw (LMS) may not be suitable for placement on the affected side. Therefore, salvage shortsegment fixation with satisfactory stability is needed when bilateral fixation is not feasible.
biomechanical tests and may play a clinical role when BPS or BMS placement is not feasible for short-segment fixation.
METHODS: Seven fresh-frozen human cervical spine specimens were used to test the 3-plane range of motion (ROM) of the C4-C5 segment. Quasistatic 2-Nm flexibility testing was performed in the following sequence: 1) intact; 2) destabilization (using 3-column injury models) treated with bilateral mass screws (BMSs); 3) destabilization treated with a unilateral PS combined with a contralateral translaminar screw (UPSDCTLS); and 4) destabilization treated with bilateral PSs (BPSs). Then, a pullout strength test was performed for the PSs, LMSs, and translaminar screws (TLSs) using 7 isolated C4 and C5 vertebrae.
INTRODUCTION
-
-
RESULTS: The UPSDCTLS group showed no significant difference from the BMS group in the 3-plane ROM or from the BPS group in the axial rotation or flexion-extension ROM but showed a significantly greater lateral bending ROM than did the BPS group. The pullout strength test showed that both C4 and C5 TLSs had strength similar to that of LMSs but poorer than that of PSs.
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CONCLUSIONS: Fixation with the hybrid UPSDCTLS construct performed as well as BMS fixation in our
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Key words Biomechanical study - Pullout strength - Range of motion - Subaxial cervical spine - Translaminar screw - Unilateral fixation -
Abbreviations and Acronyms BMS: Bilateral mass screw BPS: Bilateral pedicle screw LMS: Lateral mass screw LT: Laminar thickness PS: Pedicle screw ROM: Range of motion TLS: Translaminar screw
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P
osterior cervical screw-rod fixation is performed using pedicle screw (PS) or lateral mass screw (LMS) techniques, both of which are common for stabilization of the cervical spine.1-4 However, in several situations, such as the occurrence of tumors, fractures, or tuberculosis, the stability of the cervical spine is damaged and involves the lateral mass on 1 side; in such cases, PS or LMS placement may not be suitable on the affected side. Moreover, unilateral short-segment fixation cannot achieve sufficient biomechanical stability, and multisegment fixation over the affected level sacrifices the motion of the adjacent segment.5-7 Therefore, salvage short-segment fixation with satisfactory stability is needed when bilateral fixation is not feasible in the subaxial cervical spine. Translaminar screws (TLSs) were initially used to avoid injury to the vertebral artery (VA) that might occur during transarticular or PS fixation.8 The safety and efficacy of TLSs in C2 have been shown.9-12 Therefore, TLS placement has gained popularity as an alternative salvage technique and has been applied to the subaxial cervical and thoracic spine.13-18 Shen et al.9 proposed a novel approach consisting of unilateral C1 posterior arch screw and C2 laminar screw placement combined with an ipsilateral crossed C1-C2 PS-rod fixation technique for treating atlantoaxial
UPSDCTLS: Unilateral pedicle screw combined with contralateral translaminar screw VA: Vertebral artery Department of Orthopedics, the Second Affiliated Hospital of Chongqing Medical University, Chongqing, PR China To whom correspondence should be addressed: Zhong-Liang Deng, M.D., Ph.D. [E-mail: [email protected]; [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.09.191 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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Figure 1. Laminar screw insertion trajectory. (A) indicates the entry point, and the white arrows indicate the laminar outline under oblique fluoroscopy (axial view of lamina). (B) Cylinder simulating the translaminar screw; the tip of the screw should not
instability; this construct showed satisfactory biomechanical properties and prompted us to investigate whether we could apply hybrid unilateral fixation in the subaxial cervical spine. Because C4 and C5 have the narrowest lamina, they also have the lowest acceptance rates of 3.5-mm TLSs in the subaxial cervical spine.19-21 Therefore, we chose the C4-C5 segment as a representative segment for investigating the biomechanical properties of a novel unilateral hybrid fixation method consisting of a unilateral PS combined with a contralateral TLS (UPSþCTLS) compared with
pass the medial margin of the lateral mass (white dotted line), and the screw orientation should be parallel to the slope of the lamina under anteroposterior fluoroscopy.
traditional fixation using bilateral mass screws (BMSs) and bilateral PSs (BPSs) in cadaveric subaxial cervical spine models. METHODS Specimen Preparation After obtaining approval from the medical ethics committee of the institutional review board, 7 fresh-frozen human cadaveric cervical spine specimens (C0-C7) were obtained from 3 male and 4 female
Figure 2. Stabilization by different fixation techniques at the C4-C5 segment. (A) Bilateral mass screws. (B) Unilateral pedicle screw combined with a contralateral laminar screw. (C) Bilateral pedicle screws.
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donated cadavers and used in this biomechanical study. The mean age of the cadavers was 67 years (range, 51e78 years). Spiral computed tomography scans of each specimen (C4-C5) were obtained, and three-dimensional images were analyzed to exclude fractures and obvious degeneration or deformities. The laminar thickness (LT) of C4 and C5 was measured as the minimum thickness spanning from the ventromedial to the dorsolateral side at the central portion of the lamina bilaterally. Hence, specimens were excluded if the LT on 1 side was <3.5 mm as determined by image-based measurements. Specimens were wrapped in salinemoistened gauze, double-bagged in plastic, and frozen at e20 C. Before testing, the specimens were thawed at room temperature, and all musculature was carefully removed and all ligaments, discs, and facet joint capsules were completely preserved. Thereafter, the C0 (cranial occipital bone) and C7 vertebrae were embedded in a custom-made metal mold containing polymethylmethacrylate bone cement such that C4 was aligned horizontally. The specimens were sprayed with saline to keep them moist throughout the experiment. Biomechanical Experiments A flexibility test was first performed on all intact specimens, followed by the 3-column destabilization procedure consisting of incising the anterior longitudinal ligament, supraspinous and interspinous ligaments, facet capsules, ligamentum flavum, and posterior longitudinal ligament and completely transecting the annulus fibrosis and nucleus pulposus at C4-C5.3,16 After 3-column injury and dorsal stabilization, all 7 specimens were tested in order with BMS, UPSþCTLS, and BPS fixation. After UPSþCTLS testing, the UPS was left in place for BPS testing. Specimen Instrumentation Instrumentation applied with the implant (PCF [Wego Co., Weihai, Shandong, China]) included a titanium alloy system consisting of 3.2-mm rods and self-tapping multiaxial screws with an outer diameter of 3.5 mm. To achieve reliable screw positioning, screw insertion was performed under C-arm fluoroscopy. For PS placement, we first used landmarks to locate the entry points of the pedicle22 and then used a high-speed drill to open the entry cortex. The standard process for pedicle insertion was then performed. The optimal screw length close to the anterior cortex of the vertebral body was determined in the preoperative planning of the screw trajectories. The screws were 26e32 mm long. For LMS placement, we used the technique described by Magerl.2,3 The screw length was chosen to achieve bicortical fixation with 2 screw threads penetrating the anterior cortex. Before screw insertion, the correct drilling position was verified by manual palpation with a dissector, followed by the insertion of 3. 5-mm-diameter screws. The screws were 12e16 mm long. For TLS placement, the screw entry point was located at the initiation of the lamina from the spinous process at the midpoint of its dorsal arch. A high-speed drill was used to open the entry cortical window. Using a thin pedicle finder, the contralateral lamina was carefully drilled along its length, with the pedicle finder aimed at the lateral mass. Procedures were performed under oblique cervical fluoroscopy (axial view of the lamina) to confirm that the pedicle finder did not violate the inner cortex of
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Figure 3. Pullout strength test. Vertebral bodies were embedded individually in polymethylmethacrylate cement. The pullout test was performed along the axis of the screw at a loading rate of 2 mm/minute.
the lamina. Typically, the tip of the screw should not pass the medial margin of the lateral mass, and its orientation should be parallel to the slope of the lamina under anterior-posterior fluoroscopy13,14,23 (Figure 1). The screws were 18e22 mm long. For the experimental protocol, the screws were inserted into each vertebra from C4 to C5, followed by attachment of the rods (Figure 2).
Flexibility Test The range of motion (ROM) was tested with the MTS 858 Mini Bionix II test system (MTS Systems Corp., Eden Prairie, Minnesota, USA). The specimens were loaded using a testing system of cables and pulleys that applied pure moments and induced 3-plane movement, including flexion-extension, lateral bending, and axial rotation. Each movement was used in 3 loadingunloading cycles to a maximum torque of 2 Nm at a rate of 0.1 Nm/second. The loading was held constant for 10 seconds to minimize the viscoelastic effect. Two preconditioning cycles were performed, and data were recorded during the third loading cycle.24 During these tests, the relative motion between C4 and C5 was measured using a three-dimensional spine motion
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Table 1. The Range of Motion ( ) at the C4-C5 During Different Fixation Statuses Bilateral Mass Screw
Unilateral Pedicle Screw Combined with a Contralateral Laminar Screw
Testing Modes
Intact
Bilateral Pedicle Screw
Flexion-extension
16.12 8.73
15.576.93
13.783.47
11.795.69
Lateral bending
12.76 4.00
6.6 5.71*
7.55 2.92*
2.21 0.90*yz
Axial rotation
9.98 3.79
2.49 1.18*
2.22 0.99*
1.36 0.45*
*A significant difference from the intact (P < 0.05). yA significant difference from the bilateral mass screw (P < 0.05). zA significant difference from the unilateral pedicle screw combined with a contralateral laminar screw (P < 0.05).
measurement system (6 Eagle System [Motion Analysis Co., Woburn, Massachusetts, USA]) to process images to identify, locate, and calculate markers of the C4 and C5 positions in space.
Pullout Strength Test After the flexibility test, all C4 and C5 vertebrae were isolated by stripping the remaining soft tissue, and the vertebral bodies were embedded individually in custom-made molds with polymethylmethacrylate cement. The vertebrae were then fixed in the materials testing instrument (Material Testing System Inc., Minneapolis, Minnesota, USA) with their PS, LMS, or TLS attached to a custom clamp (Figure 3). To reduce mutual interference, the PS and TLS were tested on one side of each vertebra, and the LMS was tested on the other side. The maximum displacement and pullout strength were set to 10 mm and 3000 N, respectively. The screw pullout test was performed along the axis of the screw at a loading rate of 2 mm/minute until an abrupt change in the curved slope of the loading displacement was noted. The axial pullout force was defined as the peak load-to-failure.25
Figure 4. The primary stability of the different fixation techniques is represented by the average ROM in 3 loading planes (flexion/extension, lateral bending, and axial rotation). * Significant difference (P < 0.05). BMS,
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Statistical Analysis In the statistical analysis, analysis of variance with the StudentNewman-Keuls post hoc test (P < 0.05) was used to examine differences among the groups. Analyses were performed with SPSS Statistics for Windows, version 19.0 (IBM Corp., Armonk, New York, USA).
RESULTS No significant differences were observed in the flexion-extension ROM among the groups. However, the 3 fixation groups showed significantly lower ROMs than did the intact group in lateral bending and axial rotation. The UPSþCTLS group showed no significant difference from the BMS group in the 3-plane ROM. However, the UPSþCTLS and BMS groups showed significantly greater lateral bending than the BPS group. All data are presented in Table 1 and Figure 4. The pullout strength test showed that the average pullout strength values of C4 with a PS, LMS, and TLS were 553 177 N, 264 120 N and 311 152 N, respectively. The PS strength was greater than that of the LMS (P ¼ 0.002) and TLS (P ¼ 0.008). The
bilateral mass screw; BPS, bilateral pedicle screw UPSþCTLS, unilateral pedicle screw combined with a contralateral laminar screw.
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UNILATERAL FIXATION COMBINED PSS AND TLSS
Table 2. Axial Pullout Strength Pedicle Screw
Lateral Mass Screw
Translaminar Screw
C4 pullout load (N)
553 177
264 120*
311 152*
C5 pullout load (N)
585 118
247 94*
349 208*
*A significant difference from the pedicle screw (P < 0.05).
TLS strength was slightly greater but not significantly different from the LMS strength. Similar results were observed for pullout strength in C5 (Table 2).
DISCUSSION In several situations, such as the occurrence of tumors, fractures, or tuberculosis, the stability of the cervical spine can be damaged and involve the lateral mass of 1 side; in such cases, PS or LMS placement may not be suitable on the affected side. However, unilateral short-segment fixation cannot achieve sufficient biomechanical stability, and multisegment fixation over the affected level sacrifices the motion of the adjacent segment.5-7 Therefore, salvage short-segment fixation with satisfactory stability is needed when bilateral fixation is not feasible in the subaxial cervical spine. Unilateral fixation is generally used to prevent VA injury when asymmetry or unilateral occlusion is present.26 One study has shown that the incidence of VA occlusion induced by traumatic cervical spine injury is as high as 17.2%.27 Moreover, VA injury has been directly linked to intraoperative or perioperative death when the VA communicates only unilaterally with the basilar artery or has an obviously dominant side. In this situation, even proficient surgeons cannot guarantee 100% accuracy in PS or LMS placement without slight violation of the VA, although the rates of injury are low.28,29 Therefore, the TLS technique, as it was initially designed, is the safest for avoiding violation of the VA. The TLS technique is used to avoid injury to the VA that might occur during transarticular or PS fixation in C2 and was first described by Neill Wright in 2004.4 The TLS technique gained popularity as an alternative salvage technique and was then expanded to the subaxial cervical and thoracic spine.13-18 Shen et al.9 proposed a novel approach consisting of unilateral C1 posterior arch screw and C2 laminar screw placement combined with an ipsilateral crossed C1-C2 PS-rod fixation technique for treating atlantoaxial instability. The technique used 1-sided fixation, and the construct showed satisfactory biomechanical properties equal to those of BPSs. This development prompted us to investigate whether we could apply hybrid unilateral fixation to the subaxial cervical spine as an alternative salvage technique when bilateral fixation is not feasible. To the best of our knowledge, no previous studies using a hybrid technique in the subaxial cervical spine have been reported in the literature. Before the clinical application of this technique, biomechanical studies should be performed to examine the resulting biomechanical properties and show the feasibility of the technique. Furthermore, bilateral
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Figure 5. Notching technique. Place the screw through the basilar part of the spinosus process to the lamina, notch the outside of the lamina, and place the screw within the notch into the lateral mass.
fixation requires dissection of the posterior cervical musculature, resulting in increased invasiveness. In contrast, unilateral fixation reduces the disruption of the soft tissue, potentially reducing postoperative muscular dysfunction, pain, and disability.30 The use of LMSs is more popular than that of PSs in the subaxial cervical spine because of the superior safety and efficacy. However, the effective length of LMSs is shorter than that of PSs. This drawback resulted in unsatisfactory biomechanical stability in 3-column destabilization cervical models in the preliminary experiment. This is the main reason why we did not choose to use a construct of LMSs and TLSs. In addition, PS and TLS placement can be observed by oblique fluoroscopy; the screws are parallel to each other, and the rod can be easily inserted and placed. The clinical application of TLSs in the subaxial cervical spine is limited because of the narrowness of the lamina. Alvin et al.19 found that C5 had the smallest LT in the subaxial spine, followed by C4, and C3-C5 showed lower mean unilateral translaminar 3.5-mm screw acceptance rates (<52%). Ji et al.21 found a higher likelihood of successful TLS placement in a Korean population than in an American population. Therefore, TLSs are of limited value as a salvage technique when used in clinical situations in which bilateral fixation is not suitable. However, how should cases in which the LT is <3.5 mm be addressed? It might be appropriate to use a smaller screw diameter or a notching technique to place the screw through the basilar part of the spinosus process to the lamina, notch the outside of the lamina, and place the screw within the notch into the lateral mass (Figure 5). In the ROM tests, we calculated the total values of both directions on 1 plane of movement to minimize error. The data showed no significant differences in the flexion-extension ROM among the groups. We speculate that the reason for this lack of
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ORIGINAL ARTICLE LEI SHI ET AL.
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difference was that the cervical spine has the largest flexionextension ROM and because 3-column injury cadaveric models are unstable, increasing the difficulty of achieving sufficient biomechanical stability with posterior fixation. Moreover, UPSþCTLS versus BMS fixation showed no significant differences in the 3-plane ROM or pullout strength, although the average values were greater for UPSþCTLS fixation. Therefore, we deemed that the UPSþCTLS construct has biomechanical properties similar to those of the BMS construct. Compared with BPS, UPSþCTLS showed no significant differences in the axial rotation or flexion-extension ROM but showed a significantly greater lateral bending ROM. These data indicate that it is difficult to achieve rigid stability comparable to that of BPS via 1-sided fixation with the UPSþCTLS construct. The TLS pullout strength was also significantly poorer than the PS pullout strength. Our study has validated the feasibility of the UPSþCTLS construct by biomechanical testing. However, this study has some limitations. First, the sample size was limited by the number of
REFERENCES 1. Kothe R, Ruther W, Schneider E, Linke B. Biomechanical analysis of transpedicular screw fixation in the subaxial cervical spine. Spine (Phila Pa 1976). 2004;29:1869-1875. 2. Xu R, McGirt MJ, Sutter EG, Sciubba DM, Wolinsky JP, Witham TF, et al. Biomechanical comparison between C-7 lateral mass and pedicle screws in subaxial cervical constructs. Presented at the 2009 Joint Spine Meeting. Laboratory investigation. J Neurosurg Spine. 2010;13:688-694. 3. Bozkus H, Ames CP, Chamberlain RH, Nottmeier EW, Sonntag VK, Papadopoulos SM, et al. Biomechanical analysis of rigid stabilization techniques for three-column injury in the lower cervical spine. Spine (Phila Pa 1976). 2005;30: 915-922. 4. Jones EL, Heller JG, Silcox DH, Hutton WC. Cervical pedicle screws versus lateral mass screws. Anatomic feasibility and biomechanical comparison. Spine (Phila Pa 1976). 1997;22:977-982. 5. Ando K, Imagama S, Ito Z, Kobayashi K, Ukai J, Muramoto A, et al. Unilateral instrumented fixation for cervical dumbbell tumors. J Orthop Surg Res. 2014;9:2. 6. Bhatia N, Rama A, Sievers B, Quigley R, McGarry MH, Lee YP, et al. Biomechanical Evaluation of unilateral versus bilateral C1 lateral mass-C2 intralaminar fixation. Global Spine J. 2017; 7:239-245. 7. Riesenburger RI, Potluri T, Kulkarni N, Lavelle W, Roguski M, Goel VK, et al. Unilateral cervical facet dislocation: a biomechanical study of several constructs including unilateral lateral mass fixation supplemented by an interspinous cable. J Neurosurg Spine. 2012;16:251-256. 8. Wright NM. Posterior C2 fixation using bilateral, crossing C2 laminar screws: case series and technical note. J Spinal Disord Tech. 2004;17: 158-162.
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cadaver donations, and some specimens with a narrow LT were excluded by computed tomography examinations before testing. The fixation fatigue test was not completed because of the small sample size. Therefore, we could not examine long-term stability. Second, the pullout strength test was performed after the ROM test, which may result in underestimation of the true pullout strength. It is difficult to translate the results of biomechanical studies of any type into general clinical conclusions. Although we acknowledge the highly unstable nature of this model, the data obtained from the biomechanical tests can be used a reference for clinical usage. CONCLUSIONS Fixation with the hybrid UPSþCTLS construct performed as well as BMS fixation in our biomechanical tests and may play a clinical role when BPS or BMS fixation is not feasible for short-segment fixation.
9. Shen K, Deng Z, Yang J, Liu C, Zhang R. Biomechanical study of novel unilateral C1 posterior arch screws and C2 laminar screws combined with an ipsilateral crossed C1-C2 pedicle screw-rod fixation for atlantoaxial instability. Arch Orthop Trauma Surg. 2017;137:1349-1355. 10. Guo-Xin J, Huan W. Unilateral C-1 posterior arch screws and C-2 laminar screws combined with a 1side C1-2 pedicle screw system as salvage fixation for atlantoaxial instability. J Neurosurg Spine. 2015: 1-6. 11. Du S, Ni B, Lu X, Xie N, Guo X, Guo Q, et al. Application of unilateral C2 translaminar screw in the treatment for atlantoaxial instability as an alternative or salvage of pedicle screw fixation. World Neurosurg. 2017;97:86-92. 12. Dorward IG, Wright NM. Seven years of experience with C2 translaminar screw fixation: clinical series and review of the literature. Neurosurgery. 2011;68:1491-1499 [discussion: 1499]. 13. Shin SI, Yeom JS, Kim HJ, Chang BS, Lee CK, Riew KD. The feasibility of laminar screw placement in the subaxial spine: analysis using 215 three-dimensional computed tomography scans and simulation software. Spine J. 2012;12:577-584. 14. Cho W, Le JT, Shimer AL, Werner BC, Glaser JA, Shen FH. Anatomy of lamina in the subaxial cervical spine with the special reference to translaminar screws: CT and cadaveric analysis with screw trajectory simulation. Clin Spine Surg. 2017; 30:E535-E539. 15. Cho W, Le JT, Shimer AL, Werner BC, Glaser JA, Shen FH. The insertion technique of translaminar screws in the thoracic spine: computed tomography and cadaveric validation. Spine J. 2015;15: 309-313. 16. Kretzer RM, Hu N, Kikkawa J, Garonzik IM, Jallo GI, Tortolani PJ, et al. Surgical management of two- versus three-column injuries of the cervicothoracic junction: biomechanical comparison of translaminar screw and pedicle screw fixation using a cadaveric model. Spine (Phila Pa 1976). 2010;35:E948-E954.
17. Hong JT, An H, Park C-K, Lee SW. Significance of laminar screw fixation in the subaxial cervical spine. Spine J. 2008;8:116S-117S. 18. Jea A, Johnson KK, Whitehead WE, Luerssen TG. Translaminar screw fixation in the subaxial pediatric cervical spine. J Neurosurg Pediatr. 2008;2: 386-390. 19. Alvin MD, Abdullah KG, Steinmetz MP, Lubelski D, Nowacki AS, Benzel EC, et al. Translaminar screw fixation in the subaxial cervical spine: quantitative laminar analysis and feasibility of unilateral and bilateral translaminar virtual screw placement. Spine (Phila Pa 1976). 2012; 37:E745-E751. 20. Yusof MI, Shamsi SS. Translaminar screw fixation of the cervical spine in Asian population: feasibility and safety consideration based on computerized tomographic measurements. Surg Radiol Anat. 2012;34:203-207. 21. Ji GY, Oh CH, Park SH, Kurniawan F, Lee J, Jeon JK, et al. Feasibility of translaminar screw placement in Korean population: morphometric analysis of cervical spine. Yonsei Med J. 2015;56: 159-166. 22. Karaikovic EE, Kunakornsawat S, Daubs MD, Madsen TW, Gaines RW Jr. Surgical anatomy of the cervical pedicles: landmarks for posterior cervical pedicle entrance localization. J Spinal Disord. 2000;13:63-72. 23. Jea A, Sheth RN, Vanni S, Green BA, Levi AD. Modification of Wright’s technique for placement of bilateral crossing C2 translaminar screws: technical note. Spine J. 2008;8:656-660. 24. Tong J, Ji W, Zhou R, Huang Z, Liu S, Zhu Q. Biomechanical comparison of transfacet screws to lateral mass screw-rod constructs in the lower cervical spine. Eur Spine J. 2015;25:1787-1793. 25. Klekamp JW, Ugbo JL, Heller JG, Hutton WC. Cervical transfacet versus lateral mass screws: a biomechanical comparison. J Spinal Disord. 2000; 13:515-518.
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26. Matsubara T, Mizutani J, Fukuoka M, Hatoh T, Kojima H, Otsuka T. Safe atlantoaxial fixation using a laminar screw (intralaminar screw) in a patient with unilateral occlusion of vertebral artery: case report. Spine (Phila Pa 1976). 2007;32: E30-E33.
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screws: a systematic review. J Neurosurg Spine. 2013; 19:614-623. 29. Guan Q, Chen L, Long Y, Xiang Z. Iatrogenic vertebral artery injury during anterior cervical spine surgery: a systematic review. World Neurosurg. 2017;106:715-722.
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28. Yoshihara H, Passias PG, Errico TJ. Screw-related complications in the subaxial cervical spine with the use of lateral mass versus cervical pedicle
Conflict of interest statement: This study was supported by the Special Foundation for the Social Safeguard and
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Scientific Innovation of Chongqing (number cstc2016shmsztzx10001-6) and the Chongqing Research and Innovation Project of Graduate Students (number YB17112). Received 28 July 2018; accepted 25 September 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.09.191 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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