Comparative biomechanical study of cervical spine stabilisation by cage alone, cage with plate, or plate-cage: a porcine model

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1 Journal of Orthopaedic Surgery 2008;16(1):9-13 Comparative biomechanical study of cervical spine stabilisation by cage alone, cage with plate, or plate-cage: a porcine model J Hakalo Private Orthopaedic Practice, Swiebodzin, Poland C Pezowicz Experimental Mechanics and Biomechanics Division, Faculty of Mechanical Engineering, Wroclaw University of Technology, Wroclaw, Poland J Wronski Department of Neurosurgery, Wroclaw Medical University, Wroclaw, Poland R Bedzinski Experimental Mechanics and Biomechanics Division, Faculty of Mechanical Engineering, Wroclaw University of Technology, Wroclaw, Poland M Kasprowicz Department of Biomedical Engineering and Instrumentation, Faculty of Fundamental Problems of Technology, Wroclaw University of Technology, Wroclaw, Poland ABSTRACT Purpose. To compare stability and subsidence associated with 3 types of cervical spine stabilisation. Methods. The C3 to C4 vertebrae of 28 Polish pigs were used. Pigs with intact vertebrae (group 1) underwent standard anterior cervical discectomy (group 2), followed by stabilisation using a cage alone (group 3), a cage with plate (group 4), or a plate-cage (group 5). Cervical spine stability and subsidence were compared in all 5 groups. Results. Stability was significantly increased after stabilisation by a cage with plate or a plate-cage, but not by a cage alone. The difference between stabilisation by a cage with plate and a plate-cage was not significant. Subsidence was maximal after the cage-alone stabilisation (3.1 mm), being 1.6 mm after the cage-with-plate and plate-cage stabilisations. Conclusion. Additional plating as a supplement to anterior interbody cervical cage stabilisation significantly improves segmental stability and subsidence. Key words: biomechanics; bone plates; cervical vertebrae; diskectomy; intervertebral disk; spinal fusion INTRODUCTION Cervical plates have been used in stabilisation procedures since the early 1970s, and many biomechanical studies have confirmed their efficacy in this respect, especially for traumatic fractures. The first plates used were unconstrained 1,2 ; the Address correspondence and reprint requests to: Dr Jerzy Hakalo, Konarskiego 16, Swiebodzin, Poland. hakalo@poczta.onet.pl

2 10 J Hakalo et al. Journal of Orthopaedic Surgery Figure 1 A cervical plate-cage consists of a threaded conical interbody cage, a butterfly plate, bone screws, and a screw-blocker for connecting the plate with the cage. Figure 2 The testing machine and mounting system with a specimen during performance of a stability test. connections between the plate and screws were not blocked, enabling independent movement of the screws, causing screws to pull-out. Various screwblocking systems were introduced, but were less stable than the unconstrained system. 3 5 Stress shielding complications (pseudoarthrosis, graft osteolysis, breakage of screws or plates) cause subsidence and affect stabilisation and bone fusion. Dynamic plates were therefore developed to enable more efficient axial compressive load transfer to bone grafts so as to facilitate earlier fusion. 6,7 Good interbody stabilisation is important for anterior cervical stabilisation and load distribution of the plating systems. 8,9 Cervical interbody cages improve spinal stability, because of their mechanical durability. Plate-cages are easy to implant, clinically useful, and have fewer implant-related complications. They ensure restoration and maintenance of an interbody space height and cervical lordosis, with good stabilisation We aimed to compare stability and subsidence of 3 different types of cervical spine stabilisation (by cage alone, cage with plate, and plate-cage) after onelevel anterior cervical discectomy and fusion, carried out according to the recommendations of the German Society for Spinal Surgery. 15 MATERIALS AND METHODS 28 6-month-old Polish pigs weighing 100 to 120 kg were used. The porcine model ensures a good bone quality, consistency, and repeatability of anatomic and biomechanical conditions. Pigs with intact C3 to C4 vertebrae (group 1) were dissected and underwent standard anterior cervical discectomy with full decompression of neural elements (group 2), followed by stabilisation using a cage alone (group 3), a cage with plate (components of the plate-cage, group 4), or a plate-cage (group 5). The plate-cage (LfC Zielona Gora, Poland) consisted of a threaded conical interbody cage (16 mm in diameter), a cervical butterfly plate (28-mm long), bone screws (4 mm in diameter, 16-mm long), and a special screw blocker for connecting the plate with the cage (Fig. 1). A stability test was performed in the sagittal (flexion and extension) and frontal (right and left bending) planes of 7 specimens. The C4 vertebra was attached to the base of the MTS 858 Mini Bionix testing machine (MTS Systems, Minneapolis [MN], US) and the C3 vertebra to the gimbal (Fig. 2). The mean baseline stability of the intact vertebrae was compared with that after discectomy and that after each of the 3 types of stabilisation. The stability of the C3 vertebra was measured (in mm), with a displacement force of 2.5 Nm and speed of 40 cm/min. Six attempts were made and the results of the last 3 recorded. The Le Huec stability ratio 16 (r) was equal to the range of movement (ROM), e.g. for flexion, extension, right bending, and left bending of the intact vertebra over the ROM of the stabilised vertebra: r = ROM intact ROM stabilised A value of r<1 indicates an increase of segmental ROM after stabilisation (destabilised); r=1 indicates a lack of stabilising effect; and r>1 indicates increased stability.

3 Vol. 16 No. 1, April 2008 Comparative biomechanical study of cervical spine stabilisation 11 Table Comparison of stability ratios of intact vertebrae (baseline) with ratios after discectomy and stabilisation by a cage alone, a cage with plate, or a plate-cage Range of movement Intact vertebrae (group 1) After discectomy (group 2) Mean (SE) stability ratio Cage alone (group 3) Cage with plate (group 4) Plate-cage (group 5) p value (Tukey post-hoc test) Total range of movement 1 (0) 0.8 ( ) 1.2 ( ) 1.5 ( ) 1.6 ( ) <0.001 (groups 2 vs 5) (groups 2 vs 4) (groups 1 vs 5) (groups 1 vs 4) Flexion 1 (0) 0.8 ( ) 1.3 ( ) 2.3 ( ) 1.7 ( ) 0.01 (groups 1 vs 4) (groups 2 vs 4) Extension 1 (0) 0.6 ( ) 0.9 ( ) 0.8 ( ) 1 ( ) Not significant between Right bending Left bending groups 1 (0) 1 ( ) 1.4 ( ) 1.7 ( ) 1.7 ( ) 0.04 (groups 1 vs 3) (groups 1 vs 4) (groups 1 vs 5) 0.02 (groups 2 vs 3) (groups 2 vs 4) (groups 2 vs 5) 1 (0) 0.9 ( ) 1.3 ( ) 1.3 ( ) 2.1 ( ) Not significant between groups A subsidence test was performed in 21 specimens after stabilisation (cage alone, cage with plate, or cage-plate). The vertebrae were subjected to cycles of axial loads with a force ranging from 20 to 200 N and a frequency of 2.5 Hz. The subsidence was measured by subtracting displacements before and after the test with a 200 N preload. The extent of subsidence (in mm) between groups was compared. Analysis of variance (ANOVA) was used to evaluate the differences in mean stability ratios for each type of stabilisation. The Levene test was used to verify the assumption of homogeneity of variances; if significant, the variances were not equal across the groups. The non-parametric ANOVA (Kruskal Wallis test) was applied to verify the results. A Tukey s posthoc test was used to compare groups. A p value of 0.05 was considered significant. RESULTS The mean stability ratio of the total ROM of intact vertebrae was equal to one, it decreased to 0.8 after discectomy, and increased after stabilisation by a cage alone to 1.2, by a cage with plate to 1.5, or by a plate-cage to 1.6. Stability was significantly increased after stabilisation by a cage with plate or a platecage, but not by a cage alone. The difference between stabilisation by a cage with plate and a plate-cage was not significant. A Tukey post-hoc test showed that there were significant differences between groups 2 and 5 (p<0.001), 2 and 4 (p=0.001), 1 and 5 (p=0.006), and 1 and 4 (p=0.024). The mean stability ratios for flexion, extension, right bending, and left bending are shown in the Table. Subsidence was greatest after the cage-alone stabilisation (3.1 mm); it was 1.6 mm after the cagewith-plate and plate-cage stabilisations. The Tukey post-hoc test indicated that there were significant differences between cage-alone and cage-with-plate stabilisations (p<0.001), and cage-alone and platecage stabilisations (p=0.001). DISCUSSION Biomechanical studies using cadavers are limited and inhomogeneous with regard to age, bone mineral density, and degree of degenerative changes. Porcine specimens are widely available and ensure specimen-to-specimen consistency for comparison. 4 Biomechanical results after stabilisation on porcine and human cervical spines are similar in the sagittal plane (flexion-extension) but not in the frontal plane (lateral bending and axial rotation). 17 Thus, the results of left and right bending in our porcine model should be interpreted with caution. In human cervical spines, excision of the posterior longitudinal ligament and posterior part of uncovertebral joints causes marked segmental

4 12 J Hakalo et al. Journal of Orthopaedic Surgery destabilisation. 18,19 Our stability tests indicated that anterior cervical discectomy with removal of anterior and posterior longitudinal ligaments resulted in segmental instability, especially for extension, but the effect was not significant (p=0.09). Discectomy had the least impact on lateral bending. Instability after anterior cervical discectomy without fusion has unfavourable clinical and radiographic effects Therefore, discectomised spinal segments should be stabilised. In our study, the use of the threaded conical interbody cage for stabilisation improved overall segmental stability but not significantly (p=0.08); the result was significant only for right bending (p=0.02). The significance was associated with an absence of preliminary interbody space distraction before placement of the cage. Such distraction causes tension in the spinal ligaments and annulus fibrosus, 26 such that after release of the expanding forces adjacent bodies clump down on the cage and increase stability. 27 Most studies confirm an increase in stability with interbody cage stabilisations. Stability (ability to carry loads) is related to the distribution of loads at the cage-bone interface that depends on the shape of the cage. 28,29 In humans, it is additionally related to bone density and the extent of surgical endplate damage. Our threaded conical interbody cage supported damaged endplates and was installed without preliminary interbody space distraction. In our study, segmental stability increased significantly after additional plating, as seen in flexion and right bending, but segmental mobility was limited, which was consistent with other biomechanical and clinical studies. There was no stabilising effect in extension, probably because the plate was a dynamic one (enabling screws to move within the oval plate holes). A similar study using human lumbar spines revealed a significant (3-fold) increase of segmental stability after additional plating and a further (0.5-fold) increase after connecting the cage with the plate (plate-cage), indicating a favourable additional effect of plating after interbody cage stabilisation. 16 However, it is difficult to compare the results of that study with ours, due to differences in anatomy between human lumbar and porcine cervical spines. Subsidence is a common phenomenon in spinal surgery, because of adjustment of the cage/graft-bony bed interface Excessive subsidence can cause adverse effects, such as segmental kyphotisation, foraminal stenosis with recurrent radiculopathy, 43 and neck pain. In our study, the greatest subsidence was noted with cage-alone stabilisation; additional plating significantly decreased the extent of subsidence. With a view to minimising the risk of subsidence and spinal kyphotisation, additional plating has also been suggested for cylindrical cages. 44 REFERENCES 1. Orozco-Delclos R, Llovet-Tapies J. Osteosyntesis en les fractures de rachis cervical note de technical [in French]. Rev Ortop Traum 1970;14: Caspar W, Barbier DD, Klara PM. Anterior cervical fusion and Caspar plate stabilization for cervical trauma. Neurosurgery 1989;25: Richman JD, Daniel TE, Anderson DD, Miller PL, Douglas RA. Biomechanical evaluation of cervical spine stabilization methods using a porcine model. Spine 1995;20: Grubb MR, Currier BL, Shih JS, Bonin V, Grabowski JJ, Chao EY. Biomechanical evaluation of anterior cervical spine stabilization. Spine 1998;23: Clausen JD, Ryken TC, Traynelis VC, Sawin PD, Dexter F, Goel VK. Biomechanical evaluation of Caspar and Cervical Spine Locking Plate Systems in a cadaveric model. J Neurosurg 1996;84: Brodke DS, Gollogly S, Alexander Mohr R, Nguyen BK, Dailey AT, Bachus AK. Dynamic cervical pates: biomechanical evaluation of load sharing and stiffness. Spine 2001;26: Truumees E, Demetropoulos CK, Yang KH, Herkowitz HN. Effects of cervical compression plate on graft forces in an anterior cervical discectomy model. Spine 2003;28: Wang JL, Panjabi MM, Isomi T. The role of bone graft force in stabilizing the multilevel anterior cervical spine plate system. Spine 2000;25: DiAngelo DJ, Foley KT, Vossel KA, Rampersaud YR, Jansen TH. Anterior cervical plating reverses load transfer through multilevel strut-grafts. Spine 2000;25: Radek M, Radek A, Zapalowicz K, Maciejczak A. Anterior interbody fusion of cervical spine with cage-plate PCB [in Polish]. Neurol Neurochir Pol 2001;35: Samandouras G, Shafafy M, Hamlyn PJ. A new anterior cervical instrumentation system combining an intradiscal cage with an integrated plate: an early technical report. Spine 2001;26: Gonzalez-Darder JM, Pesudo Martinez JV, Feliu Tatay R. Post-dissectomy cervical fusion. Clinico-radiological study comparing iliac crest bone graft, anterior cervical plate with bone graft and cage-plate GD [in Spanish]. Neurocirugia (Astur) 2001;12:

5 Vol. 16 No. 1, April 2008 Comparative biomechanical study of cervical spine stabilisation Aydin MV, Sen O, Erdogan B, Sener L, Caner H, Altinors N. Anterior cervical fusion with the PCB cage-plate system. Adv Ther 2004;21: Hakalo J, Wronski J. Cervical spine stabilization by the plate-cage. Clinical evaluation. Neurol Neurochir Pol 2007;41: Wilke HJ, Wenger K, Claes L. Testing criteria for spinal implants: recommendations for the standardization of in vitro stability testing of spinal implants. Eur Spine J 1998;7: Le Huec JC, Liu M, Skalli W, Josse L. Lumbar lateral interbody cage with plate augmentation: in vitro biomechanical analysis. Eur Spine J 2002;11: Schmidt R, Richter M, Claes L, Puhl W, Wilke HJ. Limitations of the cervical porcine spine in evaluating spinal implants in comparison with human cervical spinal segments: a biomechanical in vitro comparison of porcine and human cervical spine specimens with different instrumentation techniques. Spine 2005;30: McAfee PC, Cunningham B, Dimitriev A, Hu N, Woo Kim S, Cappuccino A, et al. Cervical disc replacement-porous coated motion prosthesis: a comparative biomechanical analysis showing the key role of the posterior longitudinal ligament. Spine 2003;28:S Kotani Y, McNulty PS, Abumi K, Cunningham BW, Kaneda K, McAfee PC. The role of anteromedial foraminotomy and the uncovertebral joints in the stability of the cervical spine. A biomechanical study. Spine 1998;23: Grisoli F, Graziani N, Fabrizi AP, Peragut JC, Vincentelli F, Diaz-Vasquez P. Anterior discectomy without fusion for treatment of cervical lateral soft disc extrusion: a follow-up of 120 cases. Neurosurgery 1989;24: Sonntag VK, Klara P. Controversy in spine care. Is fusion necessary after anterior cervical discectomy? Spine 1996;21: Maurice-Williams RS, Dorward NL. Extended anterior cervical discectomy without fusion: a simple and sufficient operation for most cases of cervical degenerative disease. Br J Neurosurg 1996;10: Thorell W, Cooper J, Hellbusch L, Leibrock L. The long-term clinical outcome of patients undergoing anterior cervical discectomy with and without intervertebral bone graft placement. Neurosurgery 1998;43: Donaldson JW, Nelson PB. Anterior cervical discectomy without interbody fusion. Surg Neurol 2002;57: Hacker RJ, Miller CG. Failed anterior cervical foraminotomy. J Neurosurg 2003;98(2 Suppl):S Bagby GW. Arthrodesis by the distraction-compression method using a stainless steel implant. Orthopedics 1988;11: Schlenk RP, Stewart Todd, Benzel EC. The biomechanics of iatrogenic spinal destabilization and implant failure. Neurosurg Focus 2003;15:E Lin CY, Hsiao CC, Chen PQ, Hollister SJ. Interbody fusion cage design using integrated global layout and local microstructure topology optimization. Spine 2004;29: Tan JS, Bailey CS, Dvorak MF, Fisher CG, Oxland TR. Interbody device shape and size are important to strengthen the vertebra-implant interface. Spine 2005;30: Shimamoto N, Cunningham BW, Dmitriev AE, Minami A, McAfee PC. Biomechanical evaluation of stand-alone interbody fusion cages in the cervical spine. Spine 2001;26:E Rapoff AJ, O Brien TJ, Ghanayem AJ, Heisey DM, Zdeblick TA. Anterior cervical graft and plate load sharing. J Spinal Disord 1999;12: Pflugmacher R, Schleicher P, Gumnior S, Turan O, Scholz M, Eindorf T, et al. Biomechanical comparison of bioabsorbable cervical spine interbody fusion cages. Spine 2004;29: Hart R, Gillard J, Prem S, Shea M, Kitchel S. Comparison of stiffness and failure load of two cervical spine fixation techniques in an in vitro human model. J Spinal Disord Tech 2005;18(Suppl):S Caspar W, Geisler FH, Pitzen T, Johnson TA. Anterior cervical plate stabilization in one- and two-level degenerative disease: overtreatment or benefit? J Spinal Disord 1998;11: Geisler FH, Caspar W, Pitzen T, Johnson TA. Reoperation in patients after anterior cervical plate stabilization in degenerative disease. Spine 1998;23: Christodoulou A, Ploumis A, Terzidis I, Hantzidis P, Tapsis K, Pournaras J. Combined interbody cage and anterior plating in the surgical treatment of cervical disc disease. Acta Orthop Belg 2004;70: Song KJ, Lee KB. A preliminary study of the use of cage and plating for single-segment fusion in degenerative cervical spine disease. J Clin Neurosci 2006;13: Tye GW, Graham RS, Broaddus WC, Young HF. Graft subsidence after instrument-assisted anterior cervical fusion. J Neurosurg 2002;97(2 Suppl):S Hakalo J, Wronski J, Ciupik L. Subsidence and its effect on the anterior plate stabilization in the course of cervical spondylodesis. Part I: definition and review of literature [in Polish]. Neurol Neurochir Pol 2003;37: Hakalo J, Wronski J. Subsidence and its effect on the anterior plate stabilization in the course of cervical interbody spondylodesis. Part II. Clinical evaluation. Study design [in Polish]. Neurol Neurochir Pol 2003;37: Gercek E, Arlet V, Delisle J, Marchesi D. Subsidence of stand-alone cervical cages in anterior interbody fusion: warning. Eur Spine J 2003;12: van Jonbergen HP, Spruit M, Anderson PG, Pavlov PW. Anterior cervical interbody fusion with a titanium box cage: early radiological assessment of fusion and subsidence. Spine J 2005;5: Colpan ME, Attar A, Sekerci Z, Tuna H, Egemen N. Cervical foraminal area and intervertebral height changes after titanium ring cage placement: preliminary results. J Clin Neurosci 2006;13: Eysel P, Furderer S, Rompe JD, Zollner J. Initial instability of different cages for fusion of the cervical spine [in German]. Zentralbl Neurochir 2000;61:171 6.

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