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Clinical Biomechanics 53 (2018) 72–78

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Clinical Biomechanics
journal homepage: www.elsevier.com/locate/clinbiomech

Does pedicle screw fixation of the subaxial cervical spine provide adequate T
stabilization in a multilevel vertebral body fracture model? An in vitro
biomechanical study

John Duffa, Mir M. Hussainb, Noelle Klockeb, Jonathan A. Harrisb, , Soumya S. Yandamurib,
Lukas Bobinskia, Roy T. Daniela, Brandon S. Bucklenb
a
Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
b
Musculoskeletal Education and Research Center (MERC), A Division of Globus Medical, Inc., Audubon, PA, USA

A R T I C L E I N F O A B S T R A C T

Keywords: Background: Cervical vertebral body fractures generally are treated through an anterior-posterior approach.
Cervical Cervical pedicle screws offer an alternative to circumferential fixation. This biomechanical study quantifies
Pedicle screw whether cervical pedicle screws alone can restore the stability of a three-column vertebral body fracture, making
Lateral mass screw standard 360° reconstruction unnecessary.
Multilevel fracture
Methods: Range of motion (2.0 Nm) in flexion-extension, lateral bending, and axial rotation was tested on 10
Biomechanical
cadaveric specimens (five/group) at C2–T1 with a spine kinematics simulator. Specimens were tested for flex-
Anterior column support
ibility of intact when a fatigue protocol with instrumentation was used to evaluate construct longevity. For a
C4–6 fracture, spines were instrumented with 360° reconstruction (corpectomy spacer + plate + lateral mass
screws) (Group 1) or cervical pedicle screw reconstruction (C3 and C7 only) (Group 2).
Findings: Results are expressed as percentage of intact (100%). In Group 1, 360° reconstruction resulted in
decreased motion during flexion-extension, lateral bending, and axial rotation, to 21.5%, 14.1%, and 48.6%,
respectively, following 18,000 cycles of flexion-extension testing. In Group 2, cervical pedicle screw re-
construction led to reduced motion after cyclic flexion-extension testing, to 38.4%, 12.3%, and 51.1% during
flexion-extension, lateral bending, and axial rotation, respectively.
Interpretation: The 360° stabilization procedure provided the greatest initial stability. Cervical pedicle screw
reconstruction resulted in less change in motion following cyclic loading with less variation from specimen to
specimen, possibly caused by loosening of the shorter lateral mass screws. Cervical pedicle screw stabilization
may be a viable alternative to 360° reconstruction for restoring multilevel vertebral body fracture.

1. Introduction et al., 1994; Abumi and Kaneda, 1997; Hasegawa et al., 2008; Jeanneret
et al., 1994; Reinhold et al., 2007; Richter et al., 2000). Use of CPS has
Posterior cervical spine instrumentation is commonly used to treat not been widely adopted despite very low reported complication rates,
regional spinal instability resulting from trauma, tumor, infection, or because of associated technical difficulty and perceived risk of nerve
degenerative disease. Lateral mass screw placement remains a “gold root or vertebral artery (VA) injury (Abumi et al., 2000; Richter et al.,
standard” for posterior cervical instrumentation, with excellent results 2004). However, CPS placement is a procedure of interest, as it affords
reported (Grob and Magerl, 1987; Jeanneret et al., 1991; Roy-Camille distinct advantages over standard lateral mass screw placement
and Saillant, 1972). However, use of lateral mass screws is precluded at (Dunlap et al., 2010; Johnston et al., 2006; Jones et al., 1997; Kowalski
a vertebral level with a facet fracture, and this approach provides et al., 2000). The pullout strength of a CPS is approximately twice to
limited stabilization in patients with poor bone quality, including those quadruple that of a lateral mass screw (Ito et al., 2014; Jones et al.,
with severe osteoporosis. Placement of cervical pedicle screws (CPS) 1997). Moreover, three-column fixation can be realized through a
offers an alternative to standard lateral mass screw fixation (Abumi single posterior approach and may involve instrumentation at the level


Corresponding author at: Musculoskeletal Education and Research Center (MERC), A Division of Globus Medical, Inc., 2560 General Armistead Avenue, Audubon, PA 19403, USA.
E-mail addresses: johnmichael.duff@gmail.com (J. Duff), mhussain@globusmedical.com (M.M. Hussain), nklocke@globusmedical.com (N. Klocke),
jharris@globusmedical.com (J.A. Harris), syandamuri@gmail.com (S.S. Yandamuri), lukasbobinski@yahoo.com (L. Bobinski), roy.daniel@chuv.ch (R.T. Daniel),
bbucklen@globusmedical.com (B.S. Bucklen).

https://doi.org/10.1016/j.clinbiomech.2018.02.009
Received 28 April 2016; Accepted 12 February 2018
0268-0033/ © 2018 Elsevier Ltd. All rights reserved.
J. Duff et al. Clinical Biomechanics 53 (2018) 72–78

of an articular fracture.
Multilevel cervical vertebral body fracture (VBF) from trauma or
other pathology generally is treated by anterior reconstruction, often
supplemented by posterior stabilization (Memtsoudis et al., 2011).
However, because multilevel anterior instrumentation introduces the
potential for significant morbidity, it may be preferable to consider
treating patients with multilevel cervical VBF through a single posterior
approach with CPS placement. Although such reconstruction is plau-
sible, the basic biomechanics of a CPS construct have not been ex-
plored, and the effectiveness of CPS placement in restoring three-
column stability after disruption has not been examined.
This study looks at biomechanical aspects of two possible surgical
solutions for multilevel anterior cervical VBF. Investigators compared
the relative stability of a posteriorly placed CPS construct alone versus
360° reconstruction (with anterior cage/plate and posterior lateral mass
screw construct) before and after a simulated period of repetitive
bending (cyclic loading). Researchers hypothesized that CPS fixation,
which should maintain adequate anterior column support through in-
creased screw length, may be comparable with more invasive front-
back reconstruction. A clinical case of multilevel VBF, which could have
been treated by either of these surgical techniques, is presented later to
describe the CPS technique as used in clinical practice.

2. Methods

2.1. Specimen preparation

Ten fresh-frozen cadaveric cervical spines (two groups of five spe-


cimens) at C2–T1 were used in this study. The medical history of each
donor was reviewed along with radiographic images to exclude speci-
mens with spinal trauma, malignancy, deformity, or fracture that would
otherwise affect the outcome of the test. Specimens were then carefully
dissected, leaving only ligaments, vertebral bodies, and intervertebral
discs of desired segments. Specimens were fixed at the C2 body proxi-
mally and at the T1 body distally, using a 1:1 mixture of Bondo® Auto
Body Filler (Bondo/MarHyde Corp., Atlanta, GA, USA) and fiberglass
resin (Home Solutions™ All Purpose; Bondo/MarHyde Corp.). All spe-
cimens were double-wrapped in plastic bags and were stored at −20 °C.
Fig. 1. Custom fixture used to simulate multilevel VBF.
2.2. Fracture model and surgical reconstruction
Specimens in Group 1 had a mean age of 60.8 (standard deviation
Specimens were randomly assigned to one of two groups. To si- [SD] 10.7) years (two female, three male), and in Group 2, 65.2 (SD
mulate multilevel VBF, each specimen was placed in a custom fixture
5.8) years (three female, two male). All screws in both groups were
and loaded cranially with 5 kg to simulate the mass of the head (Fig. 1). inserted with unicortical purchase, as is common in clinical practice. An
A 3.5 mm burr tip (5100-1 TPS Console, Stryker®, Kalamazoo, MI, USA)
illustration of these groups is provided in Fig. 2.
was used to disrupt the anterior and middle columns until collapse of
the C4, C5, and C6 vertebrae, determined by visual inspection. Anterior
and posterior longitudinal ligaments were preserved at these levels. 2.3. Multidirectional and dynamic cyclic fatigue testing
After fracture creation, half of the spines were stabilized by 360° re-
construction following corpectomy of C4 through C6 with removal of Each specimen was thawed overnight and then was tested intact to
the anterior longitudinal ligament and preservation of the posterior establish baseline values. Specimens were tested for flexibility before
longitudinal ligament. Reconstruction was performed with an expand- and after a cyclic loading protocol, which was conducted to evaluate
able polyether ether ketone (PEEK) cage (XPAND®; Globus Medical, the longevity of instrumentation.
Inc., Audubon, PA, USA) at C3–7. An anterior plate (PROVIDENCE®; Researchers measured flexibility both before and after cyclic
Globus Medical, Inc.) was placed at C3–7 to restore the anterior tension loading using a custom-built six-degrees-of-freedom (6DOF) testing
band. This was followed by posterior unicortical lateral mass screw apparatus used to simulate physiological loads, as used in selected
placement (4 × 14-mm screws; ELLIPSE®; Globus Medical, Inc.) at each previous studies (Hallager et al., 2016; Kim et al., 2017; Majid et al.,
level. It is worth noting that lateral mass screws were placed at C7, as 2012; Wu et al., 2017). The cranial (C2) and caudal (T1) portion of the
each specimen was deemed to have adequately sized lateral masses at specimen was affixed via rectangular metal tubing container to a 6DOF
this level, although pedicle screws are often used at C7 in clinical motor gimbal assembly which applied a pure, unconstrained rotational
practice (Group 1). The other half of the spines were instrumented with moment independently about the x-, y-, and z-axis corresponding to
unicortical terminal point CPS (4 × 28-mm screws) at C3 and C7 but flexion-extension, axial rotation, and lateral bending. The gimbal as-
with no intermediate point fixation anchors (Group 2). All in- sembly is attached to the test platform which includes linear air-bearing
strumentation was performed under fluoroscopic guidance. A ball tip guide rails (x- and z-axis) and pneumatic-controlled linear actuator (y-
probe was used to confirm intact circumferential bone corridors with no axis) enabling pure, unconstrained translation. A load control protocol
breaches along screw trajectories. with servomotors will apply a pure moment, caudally, at a rate of 1.5°/

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J. Duff et al. Clinical Biomechanics 53 (2018) 72–78

Fig. 2. Schematic of fixation for Group 1 (360°) and Group 2 (CPS).

s, to a maximum moment of ± 2.5 Nm. Each test construct experienced


three load-unload cycles in FE, LB, and AR. Data was collected on the
third cycle to allow for the viscoelasticity of the tissue. Plexiglass strips
with three markers were placed at C3 and C7 vertebral bodies. With
these markers, relative range of motion (ROM) for all test groups was
assessed using Optotrak Certus® (Northern Digital Inc., Waterloo, ON,
Canada).
To create cyclic loading, an MTS® 858 mini bionix servo-hydraulic
machine (MTS Systems Corporation, Eden Prairie, MN, USA) was used
to simulate long-term stability in flexion-extension. Each specimen was
affixed to custom pots that were allowed to freely rotate about a pin
seated in fixtures secured at the load cell and actuator (Fig. 3). The
linear, axial motion of the actuator produced a force, and a moment was
calculated using the distance between the center of the pot and the axle.
A load-control protocol was used to apply ± 1.5 Nm at 0.75 Hz for
18,000 cycles, to simulate approximately eight weeks of maximum
bending (minor bends were ignored to obtain the worst-case scenario)
(Hedman et al., 1991). To avoid potential dehydration of the specimen
during cyclic loading, testing was performed under time constraints of
20 h, as reported by Wilke et al. (1998), so that biomechanical prop-
erties would not be affected. Specimens were wrapped in gauze and
were soaked in saline solution every 20 min throughout testing, as has
been described (Kettler et al., 2000; Wilke et al., 1998).
The two stabilization methods were compared and evaluated in
terms of ROM. Stability of the tested constructs was assessed through
measurement of peak-to-peak range of motion reported across the fix-
ated level (C3–7) and normalized to the intact condition per specimen
(intact = 100%). During ROM and cyclic fatigue, specimens were vi-
sually inspected for complications such as rod or screw fracture, screw
loosening in bone, or further induced vertebral fracture.

2.4. Case illustration

A single case was performed to assess the feasibility of bilateral


cervical pedicle screws. After experiencing severe cervical trauma from Fig. 3. Simulated in vivo cyclic fatigue test setup.
a skiing accident, a 15-year-old male presented with central cord syn-
drome with sacral sparing and bilateral distal motor deficit in the upper differences in motion (normalized to the intact condition) between
limbs (American Spinal Injury Association [ASIA] class C). experimental constructs. Two-way ANOVA was used to compare mo-
tion of independent, between-groups (test groups 1 and 2) and depen-
2.5. Data analysis dent, within-groups (tested constructs). Post hoc testing was performed
using Tukey's test with IBM SPSS® Statistics (SPSS® v22, IBM Corp.,
Statistical analysis was performed using one-factor repeated-mea- Armonk, NY, USA).
sures analysis of variance (ANOVA) to isolate significant (alpha = 0.05)

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Table 1 Table 4
360° group raw C3–C7 motion, ° (AVG ± SD). CPS group normalized C3–C7 motion, % (AVG ± SD).

Mode Intact Initial Post-fatigue Mode Intact Initial Post-fatigue

FE 23.3° (SD 10.4°) 1.8° (SD 2.0°) 5.0° (SD 5.0°) FE 100% 34.2% (SD 11.6%) 38.4% (SD 10.5%)
LB 8.3° (SD 4.2°) 0.7° (SD 0.5°) 1.0° (SD 0.8°) LB 100% 12.8% (SD 5.8%) 12.3% (SD 3.5%)
AR 21.6° (SD 9.2°) 7.6° (SD 5.8°) 9.4° (SD 9.4°) AR 100% 54.7% (SD 26.7%) 51.1% (SD 23.8%)

360° = corpectomy (C4–C6) with lateral mass screws (C3–C7). CPS = cervical pedicle screws.

Table 2
360° group normalized C3–C7 motion, % (AVG ± SD).

Mode Intact Initial Post-fatigue

FE 100% 8.0% (SD 7.7%) 21.5% (SD 18.9%)


LB 100% 9.2% (SD 9.4%) 14.1% (SD 13.9%)
AR 100% 38.0% (SD 30.3%) 48.6% (SD 53.6%)

360° = corpectomy (C4–C6) with lateral mass screws (C3–C7).

3. Results

3.1. Multidirectional and dynamic cyclic fatigue results

3.1.1. Range-of-motion
A summary of raw and normalized ROM values for 360° re- Fig. 4. Graph showing normalized range of motion for Group 1 and Group 2 with fixation
construction (Tables 1–2), raw and normalized ROM values for CPS before and after (post cycling) wear simulation. * shows statistical significance versus
intact and injured; † represents statistical differences versus Group 1 fixation before cyclic
reconstruction (Tables 3–4), and normalized ROM comparisons before
loading.
and following cyclic loading with significant relationships (Fig. 4) are
presented.
Group 1 (360°) intact specimens have average intact motion values reduced motion relative to intact, both before and after dynamic cyclic
of 23.3° (SD 10.4°) of FE, 8.3° (SD 4.2°) of LB, and 21.6° (SD 9.2°) of AR. fatigue, across all motion planes (all P < 0.05); no significant differ-
After 360° reconstruction, motion was significantly reduced to 1.8° (SD ences in motion between pre- and post-fatigue were observed (all
2.0°) FE, 0.7° (SD 0.5°) LB, and 7.6° (SD 5.8°) AR. This represents a P > 0.05) (Fig. 4). Lastly, in Group 2, screw loosening of a single right
decrease in motion to 8.0%, 9.2%, and 38.0% during FE, LB, and AR, pedicle at C7 was observed in one specimen following simulated in vivo
respectively, of intact. After cyclic loading testing, motion was in- cyclic testing.
creased in all modes to 5.0° (SD 5.0°) FE, 1.0° (SD 0.8°) LB, and 9.4° (SD
9.4°) AR, representing an increase in ROM relative to intact of 21.5%, 3.2. Case illustration results
14.1%, and 48.6% in FE, LB, and AR, respectively. Anteroposterior
reconstruction significantly reduced motion relative to intact, both Computed tomography (CT) scan showed a fracture split of the
before and after dynamic cyclic fatigue, across all motion planes (all vertebral body of C4 and C5 with kyphosis and fracture of the facet of
P < 0.05); only in FE did motion significantly increase following cyclic left C5 (Fig. 5A–C). Magnetic resonance imaging (MRI) confirmed high
fatigue (P < 0.05) (Fig. 4). Group 1 included two specimens with C7 cord signal and posterior ligamentous injury (Fig. 5D). The patient
screw loosening, observed visually during ROM testing following si- underwent stabilization through image-guided pedicle screw placement
mulated in vivo cyclic fatigue. Of the two, one specimen had loosening at C3 and C6 bilaterally with correction of kyphosis. The postoperative
of three screws (two anterior plate screws and left lateral mass screw), course was uneventful, and the patient was discharged home after two
while the other had loosening of four screws (two anterior plate screws weeks. Follow-up at two years showed fusion of the fractures (Figs. 6–7)
and both lateral mass screws). as well as posterior fusion. X-rays confirmed proper lordosis alignment
Group 2 (CPS) intact specimens have average intact motion values of the cervical spine. The patient had normal findings on neurologic
of 21.6° (SD 9.1°) FE, 9.4° (SD 3.9°) LB, and 33.3° (SD 12.2°) AR. After examination, and his daily and sporting activities were not restricted.
CPS reconstruction, motion was decreased to 7.5° (SD 3.4°) FE, 1.1° (SD
0.5°) LB, and 19.0° (SD 9.9°) AR. This represents a decrease in motion 4. Discussion
relative of intact to 34.2%, 12.8%, and 54.7% during FE, LB, and AR,
respectively. After cyclic loading testing, motion did not change much; This study was conducted to explore the stability of two different
8.0° (SD 2.9°) FE, 1.2° (SD 0.7°) LB, and 16.9° (SD 8.1°) AR, representing surgical reconstruction options for treatment of multilevel, multi-
an increase in ROM relative to intact of 38.4%, 12.3%, and 51.1% in FE, column cervical fracture. Range-of-motion baseline values indicate that
LB, and AR, respectively. Anteroposterior reconstruction significantly Group 1 (three-level corpectomy spacer + plate + lateral mass screws)
was stiffer than Group 2 (terminal pedicle screws at C3 and C7 with no
anterior reconstruction) in FE. After cyclic loading (see Fig. 4), these
Table 3
effects were somewhat neutralized, as the initially greater stiffness in
CPS group raw C3–C7 motion, ° (AVG ± SD).
Group 1 was further reduced by cyclic loading in terms of percentage to
Mode Intact Initial Post-fatigue intact than was stiffness in Group 2—ultimately resulting in near
equivalence among groups. In FE, however, Group 1 remained ~15%
FE 21.6° (SD 9.1°) 7.5° (SD 3.4°) 8.0° (SD 2.9°)
stronger than Group 2, even after cyclic loading. It remains to be seen
LB 9.4° (SD 3.9°) 1.1° (SD 0.5°) 1.2° (SD 0.7°)
AR 33.3° (SD 12.2°) 19.9° (SD 9.2°) 16.9° (SD 8.1°) whether the 15% difference in construct strength would have been
completely eliminated if cyclic loading had continued.
CPS = cervical pedicle screws. Lateral bending and AR were similar in both groups before and after

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Fig. 5. Admission computed tomography scan (CT) of A) lateral view, B) anterior-posterior view, and C) axial view shows C5 and C6 anterior and posterior fractures. Alignment is slightly
kyphotic. D) Preoperative magnetic resonance imaging (MRI) confirms high cord signal and ligamentous disruption.

cyclic testing. This shows the efficacy of CPS stabilization versus 360° 2013; Savage et al., 2011; Xu et al., 2010). Findings suggest that three-
reconstruction in these axes of motion. Moreover, AR was least affected column cervical reconstruction may be achieved through a posterior-
after fixation. Theoretically, an added cross connector may have af- only approach with placement of longer pedicle screws. Use of inter-
fected these results, as the addition of cross connectors to rigid rod mediate fixation points should further increase construct stability but
constructs has been shown to significantly reduce AR (Majid et al., was not evaluated in the current study. As posterior fusion rates of the
2011). cervical spine are generally high, anterior approaches may be re-
Comparisons of ROM following cyclic loading remain difficult due dundant (Burkhardt et al., 2013; Chen et al., 2013; Frenkel et al., 2013;
to the specificity of the operative constructs tested and lack of a defined Wang et al., 2015). Use of cervical pedicle screws is technically diffi-
standard, like the ASTM F1717, for simulating fatigue with cadaveric cult, but the difficulty may be overcome by image-guided screw pla-
specimens. Hedman et al. (1991) outlines intervertebral disc prosthesis cement, as in the presented case illustration (Bolger et al., 1999; Bolger
design considerations and estimates the average person makes 125,000 and Wigfield, 2000; Ishikawa et al., 2010; Ling et al., 2013; Mezger
“significant bends” in flexion-extension each year (Hedman et al., et al., 2013; Richter et al., 2000; Santos et al., 2012; Scheufler et al.,
1991). Tissue exposure and desiccation limits cyclic fatigue to roughly 2011a, 2011b).
18,000 cycles – at 0.75 Hz, testing requires 6.25 h to complete. Despite Results of the current study are promising with regard to insertion
this limitation, 18,000 cycles simulates approximately 7.5 weeks of of cervical pedicle screws through a posterior approach for three-
significant bends. Clinically, graft-derived cell differentiation and initial column cervical reconstruction. Although the authors cannot defini-
integration of the interbody bone graft is observed within the first two tively state that enhanced stability was due to screw length and pla-
weeks post-operatively (Gould et al., 2000). Therefore, simulating cement across the pedicle, study results appear to corroborate re-
18,000 cycles, implemented in the present study and previously by Luo sistance of cervical pedicle screws to loosening. It remains unclear at
et al. (2015), provides clinically relevant information as the patient what point enhanced initial stability of 360° fixation techniques per-
theoretically begins to heal (Luo et al., 2015). formed in a laboratory setting is nullified by gradual screw loosening.
Researchers have shown that screw purchase is relative to screw Inherent limitations of this study are common to human cadaveric
diameter and screw length (Brantley et al., 1994; Cook et al., 2004). Use studies. First, captured motion data does not account for patient factors
of much longer pedicle screws in Group 2 as compared with shorter such as bone healing. Furthermore, removal of soft tissue and the ab-
lateral mass screws in Group 1 contributed to enhanced construct sta- sence of physiologic loading of the weight of the head may have had a
bility. Several studies have confirmed the superior pullout strength of negative impact on screw loosening. Anatomic differences between
cervical pedicle screws compared with lateral mass screws (Barnes specimens could have affected results; however, all motion data was
et al., 2009; Benke et al., 2011; Dunlap et al., 2010; Kothe et al., 2004; normalized to intact to limit this influence. Lack of availability and high
Kretzer et al., 2010; Ma et al., 2009; Nassos et al., 2009; Regan et al., cost of specimens procured limited sample sizes for this study and

Fig. 6. X-rays of A) anterior-posterior view, B) flexion, and C) extension one year postoperatively.

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J. Duff et al. Clinical Biomechanics 53 (2018) 72–78

Fig. 7. Computed tomography (CT) scans of A) anterior-posterior, B) axial, and C) lateral views two years postoperatively show excellently maintained lordosis and fully healed vertebral
body fractures.

quantification of bone mineral density (BMD). The small sample size Acknowledgments
did not compromise the study within the context of cadaveric bio-
mechanical literature, which typically reports use of 3 to 8 specimens The authors would like to acknowledge editorial assistance pro-
per group (Cook et al., 2004; Kruger et al., 2012; Mundis et al., 2015; vided by Ms. Dolores Matthews, MEd, ELS, in preparation of the
Ordway et al., 2013; Santoni et al., 2013; Yeager et al., 2015a; Yeager manuscript.
et al., 2015b). Use of a larger sample size may reduce the likelihood of
type I and type II error, thereby increasing statistical power of motion References
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