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Bryan W. Cunningham, John C. Sefter, Nianbin Hu and Paul C. McAfee

Object

Using an in vivo caprine model, authors in this study compared the efficacy of autologous growth factors (AGFs) with autogenous graft for anterior cervical interbody arthrodesis.

Methods

Fourteen skeletally mature Nubian goats were used in this study and followed up for a period of 16 weeks postoperatively. Anterior cervical interbody arthrodesis was performed at the C3–4 and C5–6 vertebral levels. Four interbody treatment groups (7 animals in each group) were equally randomized among the 28 arthrodesis sites: Group 1, autograft alone; Group 2, autograft + cervical cage; Group 3, AGFs + cervical cage; and Group 4, autograft + anterior cervical plate. Groups 1 and 4 served as operative controls. Autologous growth factors were obtained preoperatively from venous blood and were ultra-concentrated. Following the 16-week survival period, interbody fusion success was evaluated based on radiographic, biomechanical, and histological analyses.

Results

All goats survived surgery without incidence of vascular or infectious complications. Radiographic analysis by 3 independent observers indicated fusion rates ranging from 9 (43%) of 21 in the autograft-alone and autograft + cage groups to 12 (57%) of 21 in the autograft + anterior plate group. The sample size was not large enough to detect any statistical significance in these observed differences. Biomechanical testing revealed statistical differences (p < 0.05) between all treatments and the nonoperative controls under axial rotation and flexion and extension loading. Although the AGF + cage and autograft-alone treatments appeared to be statistically different from the intact spine during lateral bending, larger variances and smaller relative differences precluded a determination of statistical significance. Histomorphometric analysis of bone formation within the predefined fusion zone indicated quantities of bone within the interbody cage ranging from 21.3 ± 14.7% for the AGF + cage group to 34.5 ± 9.9% for the autograft-alone group.

Conclusions

The results indicated no differences in biomechanical findings among the treatment groups and comparable levels of trabecular bone formation within the fusion site between specimens treated with autogenous bone and those filled with the ultra-concentrated AGF extract. In addition, interbody cage treatments appeared to maintain disc space height better than autograft-alone treatments.

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Masahiro Kanayama, Bryan W. Cunningham, Charles J. Haggerty, Kuniyoshi Abumi, Kiyoshi Kaneda and Paul C. McAfee

Object. Interbody fusion devices are rapidly gaining acceptance as a method of ensuring lumbar interbody arthrodesis. Although different types of devices have been developed, the comparative reconstruction stability remains controversial. It also remains unclear how different stress-shielded environments are created within the devices. Using a calf spine model, this study was designed to compare the construct stiffness afforded by 11 differently designed lumbar interbody fusion devices and to quantify their stress-shielding effects by measuring pressure within the devices.

Methods. Sixty-six lumbar specimens obtained from calves were subjected to anterior interbody reconstruction at L4–5 by using one of the following interbody fusion devices: four different threaded fusion cages (BAK device, BAK Proximity, Ray TFC, and Danek TIBFD), five different nonthreaded fusion devices (oval and circular Harms cages, Brantigan PLIF and ALIF cages, and InFix device); two different types of allograft (femoral ring and bone dowel) were used. Construct stiffness was evaluated in axial compression, torsion, flexion, and lateral bending. Prior to testing, a silicon elastomer was injected into the cages and intracage pressures were measured using pressure needle transducers.

Conclusions. No statistical differences were observed in construct stiffness among the threaded cages and nonthreaded devices in most of the testing modalities. Threaded fusion cages demonstrated significantly lower intracage pressures compared with nonthreaded cages and structural allografts. Compared with nonthreaded cages and structural allografts, threaded fusion cages afforded equivalent reconstruction stiffness but provided more stress-shielded environment within the devices.

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Bryan W. Cunningham, Nianbin Hu, Candace M. Zorn and Paul C. McAfee

Object

Using a synthetic vertebral model, the authors quantified the comparative fixation strengths and failure mechanisms of 6 cervical disc arthroplasty devices versus 2 conventional methods of cervical arthrodesis, highlighting biomechanical advantages of prosthetic endplate fixation properties.

Methods

Eight cervical implant configurations were evaluated in the current investigation: 1) PCM Low Profile; 2) PCM V-Teeth; 3) PCM Modular Flange; 4) PCM Fixed Flange; 5) Prestige LP; 6) Kineflex/C disc; 7) anterior cervical plate + interbody cage; and 8) tricortical iliac crest. All PCM treatments contained a serrated implant surface (0.4 mm). The PCM V-Teeth and Prestige contained 2 additional rows of teeth, which were 1 mm and 2 mm high, respectively. The PCM Modular and Fixed Flanged devices and anterior cervical plate were augmented with 4 vertebral screws. Eight pullout tests were performed for each of the 8 conditions by using a synthetic fixation model consisting of solid rigid polyurethane foam blocks. Biomechanical testing was conducted using an 858 Bionix test system configured with an unconstrained testing platform. Implants were positioned between testing blocks, using a compressive preload of −267 N. Tensile load-to-failure testing was performed at 2.5 mm/second, with quantification of peak load at failure (in Newtons), implant surface area (in square millimeters), and failure mechanisms.

Results

The mean loads at failure for the 8 implants were as follows: 257.4 ± 28.54 for the PCM Low Profile; 308.8 ± 15.31 for PCM V-Teeth; 496.36 ± 40.01 for PCM Modular Flange; 528.03± 127.8 for PCM Fixed Flange; 306.4 ± 31.3 for Prestige LP; 286.9 ± 18.4 for Kineflex/C disc; 635.53 ± 112.62 for anterior cervical plate + interbody cage; and 161.61 ± 16.58 for tricortical iliac crest. The anterior plate exhibited the highest load at failure compared with all other treatments (p < 0.05). The PCM Modular and Fixed Flange PCM constructs in which screw fixation was used exhibited higher pullout loads than all other treatments except the anterior plate (p < 0.05). The PCM VTeeth and Prestige and Kineflex/C implants exhibited higher pullout loads than the PCM Low Profile and tricortical iliac crest (p < 0.05). Tricortical iliac crest exhibited the lowest pullout strength, which was different from all other treatments (p < 0.05). The surface area of endplate contact, measuring 300 mm2 (PCM treatments), 275 mm2 (Prestige LP), 250 mm2 (Kineflex/C disc), 180 mm2 (plate + cage), and 235 mm2 (tricortical iliac crest), did not correlate with pullout strength (p > 0.05). The PCM, Prestige, and Kineflex constructs, which did not use screw fixation, all failed by direct pullout. Screw fixation devices, including anterior plates, led to test block fracture, and tricortical iliac crest failed by direct pullout.

Conclusions

These results demonstrate a continuum of fixation strength based on prosthetic endplate design. Disc arthroplasty constructs implanted using vertebral body screw fixation exhibited the highest pullout strength. Prosthetic endplates containing toothed ridges (≥ 1 mm) or keels placed second in fixation strength, whereas endplates containing serrated edges exhibited the lowest fixation strength. All treatments exhibited greater fixation strength than conventional tricortical iliac crest. The current study offers insights into the benefits of various prosthetic endplate designs, which may potentially improve acute fixation following cervical disc arthroplasty.

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Bryan W. Cunningham, Nadim J. Hallab, Nianbin Hu and Paul C. McAfee

Object

The introduction and utilization of motion-preserving implant systems for spinal reconstruction served as the impetus for this basic scientific investigation. The effect of unintended wear particulate debris resulting from micromotion at spinal implant interconnections and bearing surfaces remains a clinical concern. Using an in vivo rabbit model, the current study quantified the neural and systemic histopathological responses following epidural application of 11 different types of medical-grade particulate wear debris produced from spinal instrumentation.

Methods

A total of 120 New Zealand White rabbits were equally randomized into 12 groups based on implant treatment: 1) sham (control), 2) stainless steel, 3) titanium alloy, 4) cobalt chromium alloy, 5) ultra–high molecular weight polyethylene (UHMWPe), 6) ceramic, 7) polytetrafluoroethylene, 8) polycarbonate urethane, 9) silicone, 10) polyethylene terephthalate, 11) polyester, and 12) polyetheretherketone. The surgical procedure consisted of a midline posterior approach followed by resection of the L-6 spinous process and L5–6 ligamentum flavum, permitting interlaminar exposure of the dural sac. Four milligrams of the appropriate treatment material (Groups 2–12) was then implanted onto the dura in a dry, sterile format. All particles (average size range 0.1–50 μm in diameter) were verified to be endotoxin free prior to implantation. Five animals from each treatment group were sacrificed at 3 months and 5 were sacrificed at 6 months postoperatively. Postmortem analysis included epidural cultures and histopathological assessment of local and systemic tissue samples. Immunocytochemical analysis of the spinal cord and overlying epidural fibrosis quantified the extent of proinflammatory cytokines (tumor necrosis factor–α, tumor necrosis factor–β, interleukin [IL]–1α, IL-1β, and IL-6) and activated macrophages.

Results

Epidural cultures were negative for nearly all cases, and there was no evidence of particulate debris or significant histopathological changes in the systemic tissues. Gross histopathological examination demonstrated increased levels of epidural fibrosis in the experimental treatment groups compared with the control group. Histopathological evaluation of the epidural fibrous tissues showed evidence of a histiocytic reaction containing phagocytized inert particles and foci of local inflammatory reactions. At 3 months, immunohistochemical examination of the spinal cord and epidural tissues demonstrated upregulation of IL-6 in the groups in which metallic and UHMWPe debris were implanted (p < 0.05), while macrophage activity levels were greatest in the stainless-steel and UHMWPe groups (p < 0.05). By 6 months, the levels of activated cytokines and macrophages in nearly all experimental cases were downregulated and not significantly different from those of the operative controls (p > 0.05). The spinal cord had no evidence of lesions or neuropathology. However, multiple treatments in the metallic groups exhibited a mild, chronic macrophage response to particulate debris, which had diffused intrathecally.

Conclusions

Epidural application of spinal instrumentation particulate wear debris elicits a chronic histiocytic reaction localized primarily within the epidural fibrosis. Particles have the capacity to diffuse intrathecally, eliciting a transient upregulation in macrophage/cytokine activity response within the epidural fibrosis. Overall, based on the time periods evaluated, there was no evidence of an acute neural or systemic histopathological response to the materials included in the current project.

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Bryan W. Cunningham, Paul D. Sponseller, Ashley A. Murgatroyd, Jun Kikkawa and P. Justin Tortolani

OBJECTIVE

The objective of the current study was to quantify and compare the multidirectional flexibility properties of sacral alar iliac fixation with conventional methods of sacral and sacroiliac fixation by using nondestructive and destructive investigative methods.

METHODS

Twenty-one cadaveric lumbopelvic spines were randomized into 3 groups based on reconstruction conditions: 1) S1–2 sacral screws; 2) sacral alar iliac screws; and 3) S1–iliac screws tested under unilateral and bilateral fixation. Nondestructive multidirectional flexibility testing was performed using a 6-degree-of-freedom spine simulator with moments of ± 12.5 Nm. Flexion-extension fatigue loading was then performed for 10,000 cycles, and the multidirectional flexibility analysis was repeated. Final destructive testing included an anterior flexural load to construct failure. Quantification of the lumbosacral and sacroiliac joint range of motion was normalized to the intact spine (100%), and flexural failure loads were reported in Newton-meters.

RESULTS

Normalized value comparisons between the intact spine and the 3 reconstruction groups demonstrated significant reductions in segmental flexion-extension, lateral bending, and axial rotation motion at L4–5 and L5–S1 (p < 0.05). The S1–2 sacral reconstruction group demonstrated significantly greater flexion-extension motion at the sacroiliac junction than the intact and comparative reconstruction groups (p < 0.05), whereas the sacral alar iliac group demonstrated significantly less motion at the sacroiliac joint in axial rotation (p < 0.05). Absolute value comparisons demonstrated similar findings. Under destructive anterior flexural loading, the S1–2 sacral group failed at 105 ± 23 Nm, and the sacral alar iliac and S1–iliac groups failed at 119 ± 39 Nm and 120 ± 28 Nm, respectively (p > 0.05).

CONCLUSIONS

Along with difficult anatomy and weak bone, the large lumbosacral loads with cantilever pullout forces in this region are primary reasons for construct failure. All reconstructions significantly reduced flexibility at the L5–S1 junctions, as expected. Conventional S1–2 sacral fixation significantly increased sacroiliac motion under all loading modalities and demonstrated significantly higher flexion-extension motion than all other groups, and sacral alar iliac fixation reduced motion in axial rotation at the sacroiliac joint. Based on comprehensive multidirectional flexibility testing, the sacral alar iliac fixation technique reduced segmental motion under some loading modalities compared to S1–iliac screws and offers potential advantages of lower instrumentation profile and ease of assembly compared to conventional sacroiliac instrumentation techniques.

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Bryan W. Cunningham, Kyle B. Mueller, Kenneth P. Mullinix, Xiaolei Sun and Faheem A. Sandhu

OBJECTIVE

The objective of the current study was to quantify and compare the multidirectional flexibility properties of occipital anchor fixation with conventional methods of occipitocervical screw fixation using nondestructive and destructive investigative methods.

METHODS

Fourteen cadaveric occipitocervical specimens (Oc–T2) were randomized to reconstruction with occipital anchors or an occipital plate and screws. Using a 6-degree-of-freedom spine simulator with moments of ± 2.0 Nm, initial multidirectional flexibility analysis of the intact and reconstructed conditions was performed followed by fatigue loading of 25,000 cycles of flexion-extension (x-axis, ± 2.0 Nm), 15,000 cycles of lateral bending (z-axis, ± 2.0 Nm), and 10,000 cycles of axial rotation (y-axis, ± 2.0 Nm). Fluoroscopic images of the implantation sites were obtained before and after fatigue testing and placed on an x-y coordinate system to quantify positional stability of the anchors and screws used for reconstruction and effect, if any, of the fatigue component. Destructive testing included an anterior flexural load to construct failure. Quantification of implant, occipitocervical, and atlantoaxial junction range of motion is reported as absolute values, and peak flexural failure moment in Newton-meters (Nm).

RESULTS

Absolute value comparisons between the intact condition and 2 reconstruction groups demonstrated significant reductions in segmental flexion-extension, lateral bending, and axial rotation motion at the Oc–C1 and C1–2 junctions (p < 0.05). The average bone mineral density at the midline keel (1.422 g/cm3) was significantly higher compared with the lateral occipital region at 0.671 g/cm3 (p < 0.05). There were no significant differences between the occipital anchor and plate treatments in terms of angular rotation (degrees; p = 0.150) or x-axis displacement (mm; p = 0.572), but there was a statistically significant difference in y-axis displacement (p = 0.031) based on quantitative analysis of the pre- and postfatigue fluoroscopic images (p > 0.05). Under destructive anterior flexural loading, the occipital anchor group failed at 90 ± 31 Nm, and the occipital plate group failed at 79 ± 25 Nm (p > 0.05).

CONCLUSIONS

Both reconstructions reduced flexion-extension, lateral bending, and axial rotation at the occipitocervical and atlantoaxial junctions, as expected. Flexural load to failure did not differ significantly between the 2 treatment groups despite occipital anchors using a compression-fit mechanism to provide fixation in less dense bone. These data suggest that an occipital anchor technique serves as a biomechanically viable clinical alternative to occipital plate fixation.

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Charles A. Sansur, Nicholas M. Caffes, David M. Ibrahimi, Nathan L. Pratt, Evan M. Lewis, Ashley A. Murgatroyd and Bryan W. Cunningham

OBJECTIVE

Optimal strategies for fixation in the osteoporotic lumbar spine remain a clinical issue. Classic transpedicular fixation in the osteoporotic spine is frequently plagued with construct instability, often due to inadequate cortical screw–bone purchase. A cortical bone trajectory maximizes bony purchase and has been reported to provide increased screw pullout strength. The aim of the current investigation was to evaluate the biomechanical efficacy of cortical spinal fixation as a surgical alternative to transpedicular fixation in the osteoporotic lumbar spine under physiological loading.

METHODS

Eight fresh-frozen human spinopelvic specimens with low mean bone mineral densities (T score less than or equal to –2.5) underwent initial destabilization, consisting of laminectomy and bilateral facetectomies (L2–3 and L4–5), followed by pedicle or cortical reconstructions randomized between levels. The surgical constructs then underwent fatigue testing followed by tensile load to failure pullout testing to quantify screw pullout force.

RESULTS

When stratifying the pullout data with fixation technique and operative vertebral level, cortical screw fixation exhibited a marked increase in mean load at failure in the lower vertebral segments (p = 0.188, 625.6 ± 233.4 N vs 450.7 ± 204.3 N at L-4 and p = 0.219, 640.9 ± 207.4 N vs 519.3 ± 132.1 N at L-5) while transpedicular screw fixation demonstrated higher failure loads in the superior vertebral elements (p = 0.024, 783.0 ± 516.1 N vs 338.4 ± 168.2 N at L-2 and p = 0.220, 723.0 ± 492.9 N vs 469.8 ± 252.0 N at L-3). Although smaller in diameter and length, cortical fixation resulted in failures that were not significantly different from larger pedicle screws (p > 0.05, 449.4 ± 265.3 N and 541.2 ± 135.1 N vs 616.0 ± 384.5 N and 484.0 ± 137.1 N, respectively).

CONCLUSIONS

Cortical screw fixation exhibits a marked increase in mean load at failure in the lower vertebral segments and may offer a viable alternative to traditional pedicle screw fixation, particularly for stabilization of lower lumbar vertebral elements with definitive osteoporosis.

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Yasuhiro Tominaga, Travis G. Maak, Paul C. Ivancic, Manohar M. Panjabi and Bryan W. Cunningham

Object

A rotated head posture at the time of vehicular rear impact has been correlated with a higher incidence and greater severity of chronic radicular symptoms than accidents occurring with the occupant facing forward. No studies have been conducted to quantify the dynamic changes in foramen dimensions during head-turned rear-impact collisions. The objectives of this study were to quantify the changes in foraminal width, height, and area during head-turned rear-impact collisions and to determine if dynamic narrowing causes potential cervical nerve root or ganglion impingement.

Methods

The authors subjected a whole cervical spine model with muscle force replication and a surrogate head to simulated head-turned rear impacts of 3.5, 5, 6.5, and 8 G following a noninjurious 2-G baseline acceleration. Continuous dynamic foraminal width, height, and area narrowing were recorded, and peaks were determined during each impact; these data were then statistically compared with those obtained at baseline.

The authors observed significant increases (p < 0.05) in mean peak foraminal width narrowing values greater than baseline values, of up to 1.8 mm in the left C5–6 foramen at 8 G. At the right C2–3 foramen, the mean peak dynamic foraminal height was significantly narrower than baseline when subjected to rear-impacts of 5 and 6.5 G, but no significant increases in foraminal area were observed. Analysis of the results indicated that the greatest potential for cervical ganglion compression injury existed at C5–6 and C6–7. Greater potential for ganglion compression injury existed at C3–4 and C4–5 during head-turned rear impact than during head-forward rear impact.

Conclusions

Extrapolation of present results indicated potential ganglion compression in patients with a non-stenotic foramen at C5–6 and C6–7; in patients with a stenotic foramen the injury risk greatly increases and spreads to include the C3–4 through C6–7 as well as C4–5 through C6–7 nerve roots.

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Yoshihisa Kotani, Bryan W. Cunningham, Kuniyoshi Abumi, Anton E. Dmitriev, Manabu Ito, Niabin Hu, Yasuo Shikinami, Paul C. McAfee and Akio Minami

Object. This in vitro experimental study was conducted to investigate the initial biomechanical effect of artificial intervertebral disc replacement in the cervical spine. The multidirectional flexibility of replaced and adjacent spinal segments were analyzed using a cadaveric cervical spine model.

Methods. The following three cervical reconstructions were sequentially performed at the C5–6 level after anterior discectomy in seven human cadaveric occipitocervical spines: anterior artificial disc replacement with a bioactive three-dimensional (3D) fabric disc (FD); anterior iliac bone graft; and anterior plate fixation with iliac bone graft. Six unconstrained pure moments were applied with a 6-df spine simulator, and 3D segmental motions at the operative and adjacent segments were measured with an optoelectronic motion measurement system. The 3D FD group demonstrated statistically equivalent ranges of motion (ROMs) when compared with intact values in axial rotation and lateral bending. The 45% increase in flexion—extension ROM was demonstrated in 3D FD group; however, neutral zone analysis did not reach statistical significance between the intact spine and 3D FD. The anterior iliac bone graft and iliac bone graft reconstructions demonstrated statistically lower ROMs when compared with 3D FD in all loading modes (p < 0.05). The adjacent-level ROMs of the 3D FD group demonstrated nearly physiological characteristics at upper and lower adjacent levels. Excellent stability at the interface was maintained during the whole testing without any device displacement and dislodgment.

Conclusions. The stand-alone cervical 3D FD demonstrated nearly physiological biomechanical characteristics at both operative and adjacent spinal segments in vitro, indicating an excellent clinical potential for cervical artificial disc replacement.

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Bryan W. Cunningham, Brent L. Atkinson, Nianbin Hu, Jun Kikkawa, Louis Jenis, Joseph Bryant, Paul O. Zamora and Paul C. McAfee

Object

New generations of devices for spinal interbody fusion are expected to arise from the combined use of bioactive peptides and porous implants. The purpose of this dose-ranging study was to evaluate the fusion characteristics of porous ceramic granules (CGs) coated with the bioactive peptide B2A2-K-NS (B2A) by using a model of instrumented lumbar interbody spinal fusion in sheep.

Methods

Instrumented spinal arthrodesis was performed in 40 operative sites in 20 adult sheep. In each animal, posterior instrumentation (pedicle screw and rod) and a polyetheretherketone cage were placed in 2 single-level procedures (L2–3 and L4–5). All cages were packed with graft material prior to implantation. The graft materials were prepared by mixing (1:1 vol/vol) CGs with or without a B2A coating and morselized autograft. Ceramic granules were coated with B2A at 50, 100, 300, and 600 μg/ml granules (50-B2A/CG, 100-B2A/CG, 300-B2A/CG, and 600-B2A/CG, respectively), resulting in 4 B2A-coated groups plus a control group (uncoated CGs). Graft material from each of these groups was implanted in 8 operative sites. Four months after arthrodesis, interbody fusion status was assessed with CT, and the interbody site was further evaluated with quantitative histomorphometry.

Results

All B2A/CG groups had higher CT-confirmed interbody fusion rates compared with those in controls (CGs only). Seven of 8 sites were fused in the 50-B2A/CG, 100-B2A/CG, and 300-B2A/CG groups, whereas 5 of 8 sites were fused in the group that had received uncoated CGs. New woven and lamellar bone spanned the fusion sites with excellent osseointegration. There was no heterotopic ossification or other untoward events attributed to the use of B2A/CG in any group. Each B2A/CG treatment produced more new bone than that in the CG group.

Conclusions

Bioactive treatment with B2A effectively enhanced the fusion capacity of porous CGs. These findings suggest that B2A/CG may well represent a new generation of biomaterials for lumbar interbody fusion and indicate that additional studies are warranted.