The Spine Journal 12 (2012) 590–595
The importance of the posterior osteoligamentous complex to subaxial cervical spine stability in relation to a unilateral facet injury Parham Rasoulinejad, MDa, Stewart D. McLachlin, MEScb,c, Stewart I. Bailey, MDa,d, Kevin R. Gurr, MDa,d, Christopher S. Bailey, MDa,d, Cynthia E. Dunning, PhDa,b,c,* a
Division of Orthopaedics, Department of Surgery, Western University, 1151 Richmond St, London, Ontario N6A 5B9, Canada b Jack McBain Biomechanical Testing Laboratory, Thompson Engineering Building, Western University, 1151 Richmond St, London, Ontario N6A 5B9, Canada c Department of Mechanical and Materials Engineering, Western University, 1151 Richmond St, London, Ontario N6A 5B9, Canada d Orthopaedic Spine Program, Victoria Hospital, London Health Sciences Centre, 800 Commissioners Rd East - E4, London, Ontario N6A 5W9, Canada Received 17 May 2011; revised 20 January 2012; accepted 6 July 2012
BACKGROUND CONTEXT: Unilateral facet disruptions are relatively common in the cervical spine; however, the spectrum of injury is large, and little is known regarding the magnitude of instability expected to be present in an isolated posterior osteoligamentous injury. PURPOSE: To quantify the contribution of the posterior osteoligamentous structures to cervical spine stability during simulated flexion-extension (FE), lateral bend (LB), and axial rotation (AR). STUDY DESIGN: An in vitro biomechanical study. METHODS: Eight cadaveric C2–C5 spines were used in this study. A custom-developed spinal loading simulator applied independent FE, LB, and AR to the specimens at 3 /s up to 61.5 Nm. Using an optical tracking system, data were collected for the intact specimen and after sequential surgical interventions of posterior ligamentous complex (PLC) disruption, unilateral capsular disruption, progressive resection of the inferior articular process of C3 by one-half, and finally complete resection of the inferior articular process of C3. The magnitude of segmental and overall range of motion (ROM) for each simulated movement along with the overall neutral zone (NZ) was analyzed using two-way repeated-measures analyses of variance and post hoc Student-Newman-Keuls tests (a5.05). RESULTS: An increase in ROM was evident for all movements (p!.001). Within FE, ROM increased after cutting only the PLC (p!.05). For AR, sectioning of the PLC and complete bony facet fracture increased ROM (p!.05). Lateral bend ROM increased after facet capsular injury and complete articular facet removal (p!.05). There was an overall effect of injury pattern on the magnitude of the NZ for both FE (p!.001) and AR (p!.001) but not for LB (p5.6); however, the maximum increase in NZ generated was only 30%. CONCLUSIONS: The PLC and facet complex are dominant stabilizers for FE and AR, respectively. The overall changes in both ROM and NZ were relatively small but consistent with an isolated posterior osteoligamentous complex injury of the Stage I flexion-distraction injury. Ó 2012 Elsevier Inc. All rights reserved.
Spine biomechanics; Cervical spine; Instability; Range of motion; Posterior osteoligamentous complex
FDA device/drug status: Not applicable. Author disclosures: PR: Nothing to disclose. SDM: Nothing to disclose. SIB: Nothing to disclose. KRG: Nothing to disclose. CSB: Scientific Advisory Board: Stryker (A, Paid directly to institution/ employer); Research Support (Staff/Materials): Medtronic (C, Paid directly to institution/employer); Fellowship Support: Stryker (D, Paid directly to institution/employer). CED: Nothing to disclose. 1529-9430/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.spinee.2012.07.003
The disclosure key can be found on the Table of Contents and at www. TheSpineJournalOnline.com. * Corresponding author. Department of Mechanical and Materials Engineering, Spencer Engineering Building, Western University, 1151 Richmond St, London, Ontario N6A 5B9, Canada. Tel.: (519) 661-2111 ext 88306; fax: (519) 661-3020. E-mail address: [email protected]
P. Rasoulinejad et al. / The Spine Journal 12 (2012) 590–595
Introduction Unilateral facet disruptions are relatively common injury patterns of the subaxial cervical spine . However, little consensus exists among experts as to the best form of treatment [2,3]. The poor agreement stems from a combination of factors but likely includes the classification of the exact injury . A number of classification systems have been reported . The most well accepted and widely used is the Allen and Ferguson classification [5,6]. The development of these classification systems is largely based on mechanism of injury, devised from radiographic reviews, with little supporting biomechanical evidence. For the distractive-flexion mechanism, Allen et al.  classified these injuries into four stages of increasing injury severity, where a Stage I injury was defined as failure of the posterior ligamentous complex (PLC). Clinically, these isolated posterior soft-tissue injuries may also include unilateral articular process fractures. However, for specific injuries such as these, biomechanical investigations can help add depth to these classifications or treatment algorithms by providing an understanding of the instability present for specific injuries. Previous biomechanical studies have examined the stability provided by the posterior structures in the subaxial spine in the context of sectioning studies to the soft tissues, posterior laminectomy, and in advanced stages of distractiveflexion injury [7–13]. Although these studies begin to address the stabilizing role of the posterior elements, they are, for the most part, not applicable to the stability present after a traumatic Stage I distractive-flexion injury. In fact, there is a specific lack of biomechanical understanding of the stability of these injuries under the normal motions of the cervical spine and, as such, has most likely led to the controversy surrounding the most appropriate course of treatment . Thus, the purpose of this biomechanical study was to quantify the increase in motion produced after sequential disruption of the posterior osteoligamentous structures (ie, Stage I injury) based on applying simulated flexionextension (FE), axial rotation (AR), and lateral bend (LB). It was hypothesized that sequential sacrifice of the posterior stabilizing structures of the unilateral facet complex would result in progressive increase in range of motion (ROM) and neutral zone (NZ) for all simulated motions.
Proper specimen alignment was achieved with the use of laser levels to maintain C3–C4 horizontal. Fluoroscopy was used to ensure specimen integrity and appropriate screw placement. Because of the length of time required for preparation and potting, the specimens were refrozen and thawed again for testing. Repeated freezing and thawing has been shown to have little effect on the biomechanical properties of the spine . The spinal loading simulator, a custom-designed modification to an existing materials testing machine (Instron 8874; Instron Corp., Canton, MA, USA), was used to independently apply dynamic nondestructive bending moments to the spine. Loading was applied to the cranial end (C2), whereas the caudal end (C5) was fixed to the base platform of the simulator (Fig. 1). Specimens were loaded at 3 /s up to the target of 1.5 Nm to simulate movements of FE, AR, and LB [12,14]. Design of the simulator allowed for the cranial end of the spine to be free in all directions except for the movement of interest, allowing five degrees of freedom. To account for the viscoelastic effects, each movement was repeated for three complete cycles (ie, FE), with the data from the final cycle used for analysis . An Optotrak Certus optical tracking system (NDI, Waterloo, ON, Canada) was used to capture threedimensional kinematics at 60 Hz. Markers were attached
Materials and methods Eight fresh-frozen cadaveric C2–C5 cervical spines (mean age, 6869 years) were cleaned of musculature without disruption of ligaments, bones, and disc tissue. A previously described technique was used to pot the specimens at the cranial and caudal ends [14–16]. To achieve adequate fixation, screws were inserted into both C2 and C5 with the protruding ends of the screws potted within cement (Denstone; Heraeus Kulzer Inc., South Bend, IN, USA) of 1-in thickness in 4-in diameter polyvinyl chloride piping.
Fig. 1. Experimental setup. Motion was applied to cervical spine specimens (C2–C5) by means of loading arms attached to the cranial potting fixture. The caudal end of the spine was fixed to the testing platform. Axial rotation (AR) and flexion-extension (FE) could be applied in the same simulator orientation; however, lateral bend (LB) required a 90 rotation of the specimen. To capture this motion, optical tracking markers were attached in two planes (sagittal and frontal) to track FE, LB, and AR.
P. Rasoulinejad et al. / The Spine Journal 12 (2012) 590–595
to the vertebrae (C3 and C4) along two Kirschner wires. For C2 and C5, markers for both simulator orientations were attached to the cranial and caudal potting fixtures. To describe resulting kinematics along anatomical axes, a bone co-ordinate system was created with positive axes directed to anterior (x-axis), left lateral (y-axis), and superior (z-axis) and an origin at the inferior point of the midline of the vertebral body. Initially, kinematic data were collected with all ligamentous, capsular, and bony structures intact as a baseline measure for each of the three movements. Data were then captured after each stage of a sequential posterior disruption of the C3–C4 level in the following order: PLC disruption (ligamentum nuchae, interspinous, and all of the ligamentum flavum), ipsilateral (IL) facet capsular (FC) disruption, progressive resection of the inferior articular process of C3 by one-half, and finally complete resection of the inferior articular process of C3 (Fig. 2). Capsular and bony injuries were only created in the left facet for all specimens. To maintain hydration, normal saline was applied throughout the testing period. Post hoc analysis of the kinematic data generated was performed using custom-written LabVIEW software (National Instruments, Austin, TX, USA) and Euler ZYX angle algorithms . Parameters of interest included the magnitudes of overall (C2–C5) and segmental (ie, C2–C3, C3–C4, and C4–C5) ROMs as well as the NZ. The NZ measurement for each movement was defined as the width of the hysteresis curve at 60.2 Nm (Fig. 3) for C2–C5 . For ROM, separate analyses were conducted for the three movements (FE, LB, and AR). In each case, two-way analyses of variance (ANOVAs) were used to examine the effects of movement direction (eg, in the axial plane, rotating away [contralateral (CL)] or toward [IL] the injury site) and injury pattern. These were followed by post hoc Student-Newman-Keuls tests (a5.05). In contrast, the definition of NZ used in this study does not allow for
Fig. 2. A closer look at the complete bony facet removal injury (inferior facet of superior vertebrae). This bony facet was completed as the final injury step in addition to the removal of the posterior ligamentous complex and facet capsule. All bony facet cuts were completed on the left side of each specimen.
Fig. 3. Hysteresis curve. The kinematic parameters used in this study include range of motion (ROM) and neutral zone between 60.2 Nm. Both these parameters were collected from the overall motion (shown in the larger curve for axial rotation). Segmental ROM was also analyzed based on the smaller dotted curve.
directionality. Therefore, statistical analysis of NZ was performed using one-way repeated-measures ANOVA with a factor of injury stage alone. This was also followed by pairwise comparisons using post hoc Student-Newman-Keuls tests (a5.05). Results Overall kinematics (C2–C5) Differences in both ROM and NZ are provided in the Table. There was an effect of injury stage on the magnitude of the NZ for all three movements: FE (p5.001), AR (p!.001), and LB (p5.027). Within FE, the intact state was different from all injury patterns (p!.05), without significant changes between injuries. In AR, the intact and PLC disrupted states were not different from one another (pO.05), but intact was different from all the other injury states (p!.05). Although the FC cut was not different from the PLC disruption, bony resection for both the half and full cut increased NZ beyond the PLC value (p!.05). Finally, the complete bony facet removal further increased the NZ compared with the FC cut (p!.05) (Fig. 4). For the LB NZ, there was only an increase seen when the intact state was compared with the complete bony facet removal (p!.05). For ROM, the two-way repeated-measures ANOVA showed a difference for movement direction in AR only (p5.04), with more CL rotation than IL. There was also an effect of the injury state on FE (p!.001), AR (p!.001), and LB (p!.001). The FE ROM in the intact state was less than all other stages tested (p!.05). Additional removal of the bony facet increased FE ROM compared with sectioning of the PLC (p!.05), with complete bony facet removal providing a further increase compared with the FC cut (p!.05). Range of motion during AR
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Table Averaged overall ROM and NZ data Injury status
Intact PLC cut FC cut 1/2 facet Full facet
4.71 4.87 4.94 4.95 4.88
4.29 4.58 4.60 4.75 4.93
1.25 1.34 1.35 1.43 1.39
9.31 10.28 10.78 11.53 12.29
11.40 11.85 12.66 13.16 14.51
9.04 9.59 10.36 10.86 11.63
5.51 5.58 5.96 6.19 5.65
4.92 5.18 4.95 5.04 5.87
1.19 1.21 1.20 1.23 1.28
(1.15) (1.28) (1.34) (1.35) (1.26)
(1.11) (1.23) (1.42) (1.32) (1.41)
(0.38) (0.36) (0.37) (0.44) (0.37)
(2.77) (3.17) (3.38) (4.32) (4.47)
(3.18) (3.69) (4.35) (4.21) (4.11)
(2.61) (3.11) (3.81) (4.16) (4.08)
(1.13) (1.51) (1.82) (1.93) (1.66)
(1.01) (0.95) (0.82) (1.02) (1.32)
(0.25) (0.32) (0.33) (0.34) (0.37)
ROM, range of motion; NZ, neutral zone; FE, flexion-extension; AR, axial rotation; IL, ipsilateral; CL, contralateral; LB, lateral bend; PLC, posterior ligamentous complex; FC, facet capsular. Averaged ROM and NZ data are shown in degrees with the standard deviation listed along with each value in parenthesis.
increased after removal of the facet capsule over the intact state (p!.05). With bony facet involvement, further increases in ROM were seen with full facet being different from all other states and half facet resection being different from the intact and PLC cut (p!.05). In terms of the LB ROM, the only states that were not different from one another were sectioning of the PLC and FC (pO.05). Segmental kinematics For the independent segments (ie, C2–C3, C3–C4, C4–C5 only), only ROM and not NZ was considered. At the level of the injury (ie, C3–C4), there was an overall effect of injury state in FE (p!.001), AR (p!.001), and LB (p!.001), but there was no difference in movement direction (pO.05). Within FE, ROM was less for the intact stage compared with all other injury stages (p!.05) without further significant increases between injury stages (Fig. 5). Identical results were found for applied AR; however, there was also a further increase in ROM after complete inferior articular process removal compared with all other injury
Fig. 4. Overall neutral zone (NZ) for all three applied movements (ie, FE, AR, and LB) averaged over the eight specimens as a percentage of the intact NZ for the progressive injury pattern. There was a significant jump for FE after the half bony facet cut and for AR after the facet capsule removal. There was no significant change in the LB data. The starred locations represent where a significant increase occurred. FE, flexion-extension; AR, axial rotation; LB, lateral bend; PLC, posterior ligamentous complex; FC, facet capsular.
states (p!.05) (Fig. 6). Lateral bend ROM was not different between the intact and PLC cut stages (pO.05), and both were less than all other stages (p!.05). With complete inferior articular process removal, there was a further significant increase in ROM when compared with the FC cut and half bony resection stages (p!.05) (Fig. 7). For the segments above and below the injury (ie, C2–C3 and C4–C5), there was no effect of the movement direction performed and an effect of injury pattern for AR only (p5.03). In these cases, the final (full inferior articular process removal) stage had a larger ROM compared with the intact stage for both C2–C3 and C4–C5 (p!.05). There was also an increase in ROM between the final stage and PLC cut for the C2–C3 level only (p!.05).
Discussion The passive restraint provided by the posterior osteoligamentous structures to motion of the subaxial spine is not well investigated with respect to distractive-flexion injuries. This is relevant to all stages of the injury as defined by Allen et al. ; complete unilateral fracture dislocations
Fig. 5. Flexion-extension range of motion (ROM) data averaged over the eight specimens as a percentage of the intact ROM for the progressive injury pattern. There was a significant jump for flexion-extension after the posterior ligamentous complex (PLC) removal, with no large jump after this injury. The starred locations represent where a significant increase occurred. FC, facet capsular.
P. Rasoulinejad et al. / The Spine Journal 12 (2012) 590–595
Fig. 6. Axial rotation (AR) range of motion (ROM) data to ipsilateral (IL axial) and contralateral (CL axial) sides averaged over the eight specimens as a percentage of the intact ROM for the progressive injury pattern. There was a significant jump for AR after the posterior ligamentous complex (PLC) removal and again after complete bony facet removal. The starred locations represent where a significant increase occurred. FC, facet capsular.
compromise both the anterior discoligamentous support and the posterior osteoligamentous structures (Stage III or IV), whereas lesser severities of injury may represent a more isolated posterior osteoligamentous injury (Stage I) [20–22]. Previous studies by Crawford et al.  and Sim et al.  have documented injured structures, including the anterior discoligamentous restraint, necessary to achieve a unilateral facet dislocation. However, these studies represent a more severe injury than a unilateral facet injury without significant subluxation. Such an injury is not
Fig. 7. Lateral bend (LB) range of motion (ROM) data to ipsilateral (IL LB) and contralateral (CL LB) sides averaged over the eight specimens as a percentage of the intact ROM for the progressive injury pattern. There was a significant jump for LB after the facet capsule removal and again after complete bony facet removal. The starred locations represent where a significant increase occurred. PLC, posterior ligamentous complex; FC, facet capsular.
an uncommon presentation of the flexion-distraction spectrum of injury . To the authors’ knowledge, this is the first dynamic cervical spine study to quantify the passive restraint contributed by the posterior osteoligamentous structures in the subaxial cervical spine. The aim was to specifically determine the relative importance of the posterior osteoligamentous complex in controlling subaxial motion as defined by ROM and NZ parameters. The present study demonstrated that the effect of progressive sectioning was dependent on the direction of motion. This suggests that certain posterior structures are more relevant restraints to specific motions (ie, AR or flexion) than others. The dominant restraint for rotation in the sagittal plane (flexion) appears to be the PLC, which in this study represents the ligamentum nuchae, interspinous, and ligamentum flavum. This is the only structure that when sacrificed significantly increased segmental FE motion and NZ. For AR, the facet capsule and inferior articular process provide significant restraint to segmental and overall ROM as well as NZ. Neutral zone and segmental AR also increased with sacrifice of the PLC. Understandably, the CL axial motion was more significantly affected compared with IL axial motion, which relates to the morphology of the facet (the inferior articular process rests posterior to the superior articular process). No specific structure was demonstrated to be the dominant restraint for LB. As this study models an isolated posterior column injury, the magnitudes of change in ROM between the different states of sectioning were relatively moderate and did not lead to more than Stage I instability (ie, did not produce a unilateral facet dislocation) . These data demonstrate that the role of the posterior soft tissues and bony anatomy is in limiting ROM, rather than contributing to primary stability (stabilization of the spinal column). Measuring the ‘‘NZ’’ is the most widely reported method for determining the instability of the spine [14,16,18,23]. In the present study, statistical analysis showed that there was an increase in NZ with sectioning of posterior stabilizers for all three planes of rotation. However, the magnitude of the NZ measured for all motions was relatively small, although the change was statistically significant. Although NZ will increase by two to three times its original size when tested after the reduction of a unilateral subaxial facet dislocation , the maximum percentage increase in NZ generated in the present study (without creating a dislocation) was at most approximately 30% in the case of AR. Although the posterior osteoligamentous structures influence NZ stability to some degree, the spine remains relatively stable when they are compromised in isolation from the anterior discoligamentous structures. Interestingly, although NZ is generally used as the measure of stability, it has been recognized as a measure of the laxity or degeneration of the intervertebral disc . As such, the isolated posterior osteoligamentous injury states created in this study would not be expected to significantly impact
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the NZ measure and help to explain the observations seen in this work. There are inherent limitations related to the in vitro nature of the study. There was a large variability in terms of the measured ROM and NZ between specimens, evident by the relatively large standard deviations. This is likely the result of significant specimen variability, in terms of soft-tissue quality and disc degeneration; however, the effect of this variability is limited by the repeated-measures design of the study, which allowed for the injury progression to be compared within the same specimen. On the other hand, the repeated-measures design only allowed for one injury progression model to be evaluated for our sample size, which was feasibly limited to testing eight specimens. Although a different sequence of injury progression is clinically possible, our sectioning protocol represents a reasonable attempt to model the injury progression of an isolated posterior column injury after a flexion-distraction mechanism. Furthermore, the authors chose to investigate only one injury level (C3–C4) along with one segment above and below the injury; however, different results may have been seen with an injury to a lower motion segment. The load target of 1.5 Nm used in this study was based on previous studies that have attempted to measure cervical spine stability [12,14]. In the present study, the ROM produced by this value was less than expected. However, our initial pilot study showed the same relative changes between injury stages at higher load targets; therefore, the widely reported value was chosen. In conclusion, disruption of the posterior osteoligamentous structures of the C3–C4 motion segment leads to an increase in ROM for all three planes. The PLC and facet complex are dominant stabilizers for FE and AR, respectively. The overall changes in both ROM and NZ were relatively small but consistent with an isolated posterior osteoligamentous complex injury of the Stage I flexiondistraction injury. To further understand the entire ‘‘spectrum of instability’’ surrounding unilateral facet fracture/dislocations, future studies should be performed to understand the elastic/plastic deformation of the anterior discoligamentous complex with and without an associated posterior osteoligamentous injury.
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