SPINE Volume 39, Number 11, pp E684-E692 ©2014, Lippincott Williams & Wilkins
BIOMECHANICS
Biomechanical Evaluation of a Novel Autogenous Bone Interbody Fusion Cage for Posterior Lumbar Interbody Fusion in a Cadaveric Model Le Wang, MS,* Kyle T. Malone, MS,† Hai Huang, MS,* Zhenshan Zhang, MS,* Zhi Zhang, MD,* Liang Zhang, MD,* and Jian Li, MD, PhD*
Study Design. A human cadaveric biomechanical study of a novel, prefabricated autogenous bone interbody fusion (ABIF) cage. Objective. To evaluate the biomechanical properties of the ABIF cage in a single-level construct with and without transpedicular screw and rod fixation. Summary of Background Data. In current practice, posterior lumbar interbody fusion is generally carried out using synthetic interbody spacers or corticocancellous iliac crest bone graft (ICBG) in combination with posterior instrumentation. However, questions remain concerning the use of synthetic intervertebral implants as well as the morbidity ICBG harvesting. Therefore, ABIF cage has been developed to obviate some of the challenges in conventional posterior lumbar interbody fusion instrumentation and to facilitate the fusion process. Methods. Eighteen adult cadaveric lumbosacral (L3–S1) specimens were tested. Test conditions included single lumbosacral segments across (1) intact, (2) decompressed, (3) intervertebral cage alone, and (4) intervertebral cage with bilateral transpedicular fixation. Range of motion (ROM), neutral zone (NZ), and axial failure load were tested for each condition. Results. The ICBG, polyetheretherketone cage, or ABIF cage alone exhibited a significantly lower (P < 0.05) ROM and NZ than the decompressed spine. In comparison with the intact spine, all 3 test conditions without supplemental fixation were able to decrease ROM and NZ to near intact levels. When stabilized with pedicle screws, the ROM was significantly less and the NZ was significantly From the *Institute of Orthopaedics and Traumatology, the Third Affiliated Hospital, Guangzhou Medical University, People’s Republic of China; and †NNI Research Foundation, Las Vegas, NV. Acknowledgment date: September 18, 2013. First revision date: January 13, 2014. Second revision date: February 9, 2014. Acceptance date: February 12, 2014. The device(s)/drug(s) that is/are the subject of this manuscript is/are not FDA approved for this indication and is/are not commercially available in the United States. National Natural Science Foundation of China (No.31200726) grant funds were received to support this work. Relevant financial activities outside the submitted work: grant. Address correspondence and reprint requests to Jian Li, MD, PhD, Institute of Orthopaedics and Traumatology, the Third Affiliated Hospital, Guangzhou Medical University, 63, Duobao Rd, Guangzhou, 510150, People’s Republic of China; E-mail: [email protected] DOI: 10.1097/BRS.0000000000000291
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lower (P < 0.05) for each group both compared with the intact spine. In axial compression testing, the failure load of polyetheretherketone cage was the highest, with no significant difference between the ICBG and the ABIF cage. Conclusion. These data suggest that the novel ABIF cage can bear the physiological intervertebral peak load, similar to ICBG. When combined with pedicle screw and rod fixation, it exhibits similar biomechanical properties as the polyetheretherketone cage plus posterior instrumentation. Based on the biomechanical properties of ABIF cage, the prospect of these cages in clinical practice is expected. Key words: posterior lumbar interbody fusion, autogenous bone, cage, pedicle screws. Level of Evidence: N/A Spine 2014;39:E684–E692
P
osterior lumbar interbody fusion (PLIF) is a wellestablished surgical procedure in treatment of a variety of lumbar degenerative conditions since its introduction by Jaslow1 and subsequent modification by Cloward.2,3 The surgical goals of PLIF are to provide a solid fusion with direct neural decompression, to restore normal disc height, realign spinal segment, and provide an adequate fusion environment, thereby hastening postoperative rehabilitation and fusion process.4 In general, PLIF is performed using synthetic intervertebral cages with autogenous bone, corticocancellous iliac crest bone graft (ICBG), or other bone graft material implanted in the intervertebral space. However, previous studies have reported several complications in the use of synthetic cages, including risk for subsidence and corrosive effects, which have recently been noted to contribute to an increasing incidence of revision surgery.5,6 In addition, cages still require bone graft material and do not incorporate as part of the fusion mass, which may create immunological problems.7,8 Moreover, harvesting autologous bone graft from iliac crest is associated with a significant morbidity that can occur in as many as 30% to 40% of patients.9,10 In an effort to resolve such problems of mechanical cage devices and morbidity of ICBG, Simmons11 developed the concept of harvesting corticocancellous autologous bone from the posterior elements of vertebra being treated itself.
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BIOMECHANICS When spinal cord was decompressed, the lamina and spinous process were cut into small corticocancellous chips and subsequently used as graft material. These corticocancellous chips were used to fill in the intervertebral space for facilitation of fusion. In a retrospective study, Turner et al12 found that PLIF with such corticocancellous chips provided the highest fusion rate and the most satisfactory clinical results. However, some problems such as collapse and pseudarthrosis have been reported when these bone grafts were used.13 Furthermore, one of the major problems is that such bone graft cannot provide sufficient mechanical strength compared with ICBG or synthetic cages. To avoid the collapse of these bone grafts and to satisfy the biological requirements of spinal fusion, a machine designed to compress and prefabricate a novel cage consisting of morselized autogenous bone was developed by the authors of current study. This implant has been designated as an autogenous bone interbody fusion (ABIF) cage. As ABIF cage is a novel implant, no biomechanical or testing has been published to compare its mechanical properties with alternative cages. The purpose of this study was to analyze the axial compression properties of ABIF cage and to evaluate the biomechanical characteristics of this novel cage in comparison with ICBG and polyetheretherketone (PEEK) cages in a single-level of lumbar spine.
MATERIALS AND METHODS Specimen Preparation Eighteen fresh-frozen L3–S1 spine segments and ICBGs were obtained from the department of Pathology, Guangzhou Medical University, for use in the current biomechanical testing. Mean specimens’ age was 50 years (standard deviation: 8.9 yr, range: 35–65 yr) and were made up of 7 males and 11 females. Ethics committee approval for use of the specimens was granted by the ethics committee of Guangzhou Medical University. All specimens were radiographed for any abnormalities or spinal fractures. As bone quality is always a concern in such laboratory testing,14 dual-energy x-ray absorptiometry was performed in anterior posterior direction to measure the bone mineral density (BMD) of each vertebra. The spinal segments were stored in a freezer at −20°C. Before testing, the spine was thawed and kept moistened with saline. The L3–S1 segments were used in all range of motion (ROM)
Biomechanical Evaluation; a Novel Cage • Wang et al
and neutral zone testing, although the L4–L5 level was the only level treated. In addition, the L4–L5 was a separate functional spinal unit in the axial compression test.
ABIF Cage Preparation ABIF cage is fabricated in 2 steps. The first step involves preparation of raw materials. When spinal cord is decompressed during the PLIF procedure, the lamina and spinous process are cut into small corticocancellous chips measuring 2 to 4 mm (Figure 1A–D). The second step involves placement of these harvested local corticocancellous chips into a cageshaped groove at the bottom of a specialized machine (China Pat. No. ZL201120261348.8), which can generate enough vertical pressure by twisting a rotatable handle and compact the corticocancellous chips into ABIF cage. Preparation of an ABIF cage took 3.0 g corticocancellous chips, which was measured by electronic balance. The configuration of this cage was followed the design of standard PEEK cage (Wego Holding Co Limited, Weihai, China), and the implant dimensions were 16 × 6 × 13 mm (length × height × width). The configurations of ABIF cage, PEEK cage, and ICBG are showed in Figure 2. In addition, the BMD of the ABIF cages and the ICBG were measured by dual-energy x-ray absorptiometry as a reference.
Testing
Each L3–S1 specimen (n = 18) served as its own control and was tested in the following sequence (Figure 3): (1) intact (control group, n = 18) and (2) decompressed (post L4–L5 laminectomy, including medial facetectomy involving 50% of the facet joint and resection of the posterior longitudinal ligaments, n = 18). After testing on conditions 1 and 2, all specimens were randomly assigned to one of the following test conditions for evaluation of interbody cage stiffness using ICBG (n = 6), PEEK cage (n = 6), or ABIF cage (n = 6) at L4-–L5. After interbody cage stiffness testing, each L4–L5 segment within L3–S1 construct was additionally stabilized with pedicle screws (Wego Holding Co Limited, Weihai, China) (each group, n = 6). To ensure consistency in the procedure performed between specimens, a single surgeon performed all decompression and PLIF procedures. In addition, the failure loads of ICBGs, ABIF cages, and PEEK cages were evaluated in L4–L5 segments alone through an axial compression test (each group, n = 6).
Figure 1. A series of images showing the process of autogenous bone interbody fusion (ABIF) cage preparation. Small corticocancellous bones were obtained from the posterior decompression performed prior to posterior lumbar interbody fusion (A). Using a specialized compressive machine (China Pat. No. ZL 2011 2 0261348.8 [21 Mar 2012]), the raw materials were prefabricated into the ABIF cage (B and C). Images showing the ABIF cage (D). Spine
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Biomechanical Evaluation; a Novel Cage • Wang et al
Figure 2. Superior and lateral views of iliac crest bone graft (A). Images showing the dimensions of the autogenous bone interbody fusion cage (B). Superior and lateral views of a polyetheretherketone cage (C).
Stiffness Testing The L3 and S1 vertebrae were set in polymethylmethacrylate. Each specimen was placed in a spinal loading frame capable of applying independent bending moments and axial loads (MTS 858, MTS Systems, Eden Prairie, MN) (Figure 4). The spine simulator consisted of an axial torsion actuator and 2 rotational actuators for lateral bending and flexion– extension. These actuators were mounted on the upper side of the test machine. A low-friction cross roller slide table mounted on the lower side allowed pure bending moments to be applied to the specimen. After fixing the spine to an immobile base plate within the testing frame, labeled steel pins with
infrared light emitting diodes were attached to L4 and L5 vertebrae. A special set of light emitting diodes was also attached to the immobile base for reference. The 3-dimensional locations of the light emitting diodes were quantified after each loading step by a motion analysis system (VICON; Oxford Metrics, Ltd., Oxford, United Kingdom), and 3 images were obtained during each test cycle. A 100 N axial compressive preload was maintained throughout each test so as not to damage the specimens that lacked musculature and joint support, and this small preload was used in an effort to minimize the amount of artifact.15 After specimen was mounted on the spinal tester, left–right
Eighteen fresh-frozen L3–S1 spine segments in humans
(1) Intact state (n = 18)
(2) Decompressed state (n = 18)
ROM and stiffness test
(3) Autologous iliac crest bone
(4) ABIF cage
(4) PEEK cage
graft alone (n = 6)
alone (n = 6)
alone (n = 6)
(6) Iliac crest bone graft or cage combined with pedicle screws fixation (n = 6, each group)
Axial compression test
Autologous iliac crest bone graft alone (n = 6)
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ABIF cage alone
PEEK cage alone
(n = 6)
(n = 6)
Figure 3. The testing sequence of the three grafts. ROM indicates range of motion; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone
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BIOMECHANICS
Biomechanical Evaluation; a Novel Cage • Wang et al
expressed as mean ± SD. Comparison of ROM, NZ, stiffness, and failure load was performed using 1-way analysis of variance for independent samples, followed by a StudentNeumann-Keuls-q test for multiple comparisons.
RESULTS
Average BMD and T and Z scores of specimens were 1.05 ± 0.14 g/cm2, 0.44 ± 0.61, and 1.16 ± 0.69, respectively. These parameters showed nearly normal values. In addition, the BMD of the ABIF cage was reached from 0.52 to 0.62 g/cm2, with a mean of 0.58 g/cm2, and that of the ICBG was reached from 0.48 to 0.59 g/cm2, with a mean of 0.54 g/cm2. There were no statistically significant differences in BMD between these 2 grafts (P > 0.05).
ROM and Stiffness Figure 4. Image showing laboratory testing setup.
lateral bending, flexion–extension, and left–right axial rotation of the specimen with a maximum moment loads of ±6 N·m16,17 were conducted at a constant speed of 0.5° per second in sequence before and after different surgical procedures. The order of directional sequences for loading was randomized. Three cycles were applied for each loading condition, with the last cycle used for data analysis. After each test mode, the specimens were allowed to relax for 60 seconds before further data were recorded. The ROM, neutral zone (NZ), elastic zone, and the stiffness values were calculated from the corresponding load-displacement curves. In brief, the ROM was calculated between an applied load of 6 N·m and −6 N·m. The NZ was defined as the difference in angulation at load of 0 N·m between the 2 phases of motion. The elastic zone was defined from the end of the NZ to the point of the maximal loading. Stiffness in elastic zone was estimated as the inverse slope of a trend line applied to the load displacement curve at ±6 N·m. For further analysis, values were averaged over both movement directions.18
Axial Compression Test of ABIF Cage After stiffness testing, the PEEK cages, ABIF cages, and ICBG were tested in compression with the same machine. For this test, L4 and L5 vertebral bodies were potted using polymethylmethacrylate and constrained from rotation during the test. Axial compression displacement was applied at the constant speed of 5 mm/min. While applying loading, compressive force and displacement data were recorded with 25 Hz. The real-time compressive load displacement curve was electronically recorded. Finally, the compression test was continued until failure as evidenced by a drop or a split fracture in vertebral body or in the construct. The failure load was defined as the point at which further deformation resulted in a decrease of measured force.19
Data and Statistical Analysis All data were analyzed using SPSS software, and statistically significant values were defined as P < 0.05. The data were Spine
Compared with intact spine and all subsequent test conditions, the mean ROM of decompressed state was statistically significantly higher (P < 0.05), especially in flexion–extension. In comparison with decompressed state, the addition of ICBG, PEEK cage, or ABIF cage alone was able to reduce ROM and NZ to near intact levels (P < 0.05). Meanwhile, the mean angular displacement value in lateral bending was still slightly greater than intact spine but was not statistically significant. The ROM and NZ of PEEK cage alone group were slightly lower than those of ICBG or ABIF cage alone group. However, the difference was not statistically significant. This meant that no single cage or bone graft was statistically different from any of the others. Intuitively, compared with the cage or bone graft alone groups, the groups stabilized with posterior pedicle screws demonstrated a significantly lower (P < 0.05) ROM and NZ in all planes of motion. In addition, there were no statistically significant differences in ROM of NZ between groups (ABIF, PEEK, or ICBG stabilized with pedicle screws [P > 0.05]) (Table 1). The stiffness data of each group were normalized to the intact state. Compared with the stiffness of intact state, the values in decompressed state were decreased in all testing conditions. In addition, there was no significant difference among ICBG, PEEK cage, and ABIF cage alone groups in all directions. Furthermore, each experimental group stabilized with pedicle screws showed significantly higher stiffness (P < 0.05) than the single cage or bone graft group (Table 2) (Figure 5).
Axial Compression Testing The real-time compressive load displacement curve for the 3 grafts was showed in Figure 6. In comparison with ICBG and ABIF groups, the failure load was significantly higher in PEEK cage group (6.83 ± 0.92 kN) (P < 0.05). In addition, all specimens exhibited a split fracture in vertebral body when using PEEK cage alone. However, as shown in Figure 7, ICBG and ABIF cage collapsed and fractured when axial compression was added. In addition, the failure load of ABIF cage (3.25 ± 0.39 kN) was slightly higher than ICBG group (2. 96 ± 0.25 kN), although there was no observed statistical difference (Table 3) (Figure 8). www.spinejournal.com
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1.15 ± 0.05
1.61 ± 0.25*
1.21 ± 0.09*†
5.36 ± 0.31*†
3.45 ± 0.65†
10.91 ± 1.52†
4.31 ± 0.47*†
14.66 ± 1.32*†
ICBF Alone
1.18 ± 0.08*†
5.30 ± 0.38*†
3.44 ± 0.58†
10.87 ± 1.64†
4.21 ± 0.50*†
14.44 ± 1.60*†
ABIF Cage Alone
1.24 ± 0.07*†
5.18 ± 0.45*†
3.35 ± 0.61†
10.75 ± 1.65†
4.25 ± 0.45*†
14.25 ± 1.25*†
PEEK Cage Alone
0.15 ± 0.02*†‡
1.21 ± 0.14*†‡
0.91 ± 0.04*†‡
2.11 ± 0.71*†‡
0.51 ± 0.08*†‡
2.91 ± 0.02*†‡
ICBF + PPSFS
0.11 ± 0.03*†‡
0.91 ± 0.05*†‡
0.83 ± 0.08*†‡
2.01 ± 0.68*†‡
0.48 ± 0.03*†‡
2.79 ± 0.06*†‡
ABIF Cage + PPSFS
0.10 ± 0.01*†‡
0.98 ± 0.09*†‡
0.82 ± 0.05*†‡
1.97 ± 0.75*†‡
0.45 ± 0.06*†‡
2.74 ± 0.05*†‡
PEEK Cage + PPSFS
2.93 ± 0.38 100 ± 13.05 5.85 ± 0.59 100 ± 10.12
Bending (N·m/degree)
Normalized (%)
Rotation (N·m/degree)
Normalized (%) 43.55 ± 10.56
2.55 ± 0.62
53.41 ± 9.21
1.56 ± 0.27
48.52 ± 12.52
1.17 ± 0.31
Decompressed
1.87 ± 0.28
ABIF Cage
2.67 ± 0.30
2.79 ± 0.43
79.60 ± 8.51
1.95 ± 0.21
PEEK Cage
5.67 ± 0.51
ABIF Cage + PPSFS
6.50 ± 0.69
6.54 ± 0.65
223.91 ± 21.04 231.44 ± 20.87
5.49 ± 0.52
ICBF + PPSFS
79.41 ± 8.02
4.65 ± 0.47
79.01 ± 7.10
4.62 ± 0.42
82.77 ± 8.11
4.84 ± 0.47
8.62 ± 0.94 145.55 ± 20.11 147.41 ± 16.12
8.51 ± 1.18
90.11 ± 11.12 91.21 ± 10.37 95.14 ± 14.84 221.95 ± 23.54 223.12 ± 22.32
2.64 ± 0.33
74.11 ± 10.41 76.51 ± 11.60
1.82 ± 0.26
ICBF
*For statistical evaluation, see text. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone; PPSFS, posterior pedicle screw fixation system.
100 ± 12.05
2.45 ± 0.31
Intact
Normalized (%)
Flexion–extension (N·m/degree)
Conditions Directions
148.24 ± 18.31
8.67 ± 1.07
234.15 ± 19.18
6.86 ± 0.56
233.04 ± 21.12
5.71 ± 0.52
PEEK Cage + PPSFS
TABLE 2. Stiffness (N·m/Degree) in the EZ of the 3 Grafts Tested in the Study in Response to Different Conditions and Directions*
*Significant difference in comparison with intact motion segment. †Significant difference in comparison with decompressed motion segment. ‡Significant difference in comparison with the cage or ICBF alone. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone; PPSFS, posterior pedicle screw fixation system; ROM, range of motion; NZ, neutral zone.
NZ
6.92 ± 1.09*
4.51 ± 0.95*
3.21 ± 0.68
4.21 ± 0.42
14.61 ± 1.58*
ROM
Rotation
NZ
ROM
5.58 ± 0.54*
19.05 ± 1.97*
Decompressed
10.31 ± 1.35
3.64 ± 0.52
NZ
Bending
12.20 ± 1.62
Intact
ROM
Flexion–extension
Test Mode (°)
extension, Rotation (Both Sides), and Bending (Both Sides) (χ ± s°)
TABLE 1. Range of Motion, Neutral Zone of the Different Bone Graft, or Cages Tested in the Study in Response to Flexion-
BIOMECHANICS Biomechanical Evaluation; a Novel Cage • Wang et al
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BIOMECHANICS
Biomechanical Evaluation; a Novel Cage • Wang et al
Figure 7. Images showing the iliac crest bone graft (A) and the autogenous bone interbody fusion cage (B) collapsed and fractured after axial compression testing. Figure 5. Graph of the stiffness results normalized to the intact motion segment in the elastic zone. *Significant difference in comparison with intact motion segment. †Significant difference in comparison with decompressed motion segment. ‡Significant difference in comparison to the cage or ICBF alone. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone.
DISCUSSION Design of ABIF Cage Rigid spinal stabilization using intervertebral cages or bone grafts with transpedicular screw instrumentation has resulted in increased fusion rates with superior clinical outcomes compared with those without supplemental internal fixation.20,21 In addition to the biomechanical properties of intervertebral spacers, their biological properties (or lack thereof) additionally factor into the final fusion construct. Autograft has significant advantages and is considered the “gold standard” for bone graft material in fusion procedures because of its inherent properties of osteoconduction, osteoinduction, and provision of a cellular component for bone healing.22 However, graft site complications and morbidity are not uncommon in harvesting autograft, including wound infection, hematoma, iliac crest fracture, and donor site pain.23–26 The variable
Figure 6. The typical load displacement curve of the 3 grafts in axial compression testing. Black arrows represent change in slope from positive to negative, indicating the failure load of each graft. PEEK indicates polyetheretherketone; ABIF, autogenous bone interbody fusion; ICBF, iliac crest bone graft. Spine
incidence of complications in using autologous bone has led to the development of synthetic intervertebral implants. Currently, although cages made of PEEK claim advantage in that its Young modulus (“E” = 3.6–4 GPa) is similar to that of cortical bone (“E” = 12 GPa),27,28 the difference still remains. Cages manufactured using medical alloys do not have the ability to promote bone ingrowth, and the cage material does not exhibit degradation in vivo.29,30 To reduce the incidence of complications in using autologous ICBG and to overcome the disadvantages of alloy cages described previously, this study evaluated implants developed using a machine to compress small corticocancellous chips, previously considered waste, to prefabricate an ABIF cage.
TABLE 3. The Demographics, BMD, and Failure
Load of Each Specimen
No.
Sex Age (yr) BMD (g/cm2) Failure Load (kN)
1. ABIF
F
45
1.09
3.10
2. ABIF
F
63
1.12
3.78
3. ABIF
F
56
0.68
2.90
4. ABIF
M
50
1.00
2.82
5. ABIF
M
58
1.08
3.63
6. ABIF
F
65
1.07
3.27
7. ICBG
F
48
1.17
3.12
8. ICBG
M
35
0.83
2.77
9. ICBG
F
45
1.03
2.67
10. ICBG
M
64
1.09
2.88
11. ICBG
M
47
1.11
2.93
12. ICBG
F
36
1.25
3.37
13. PEEK
F
46
0.89
6.29
14. PEEK
F
52
1.13
6.85
15. PEEK
M
39
1.08
7.95
16. PEEK
F
45
1.06
6.62
17. PEEK
M
54
1.26
7.76
18. PEEK
F
48
1.03
5.51
BMD indicates bone mineral density; ABIF, autogenous bone interbody fusion; F, female; M, male; ICBG, iliac crest bone graft; PEEK, polyetheretherketone.
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BIOMECHANICS
Figure 8. Graph showing the results of axial compression testing of the ICBF, ABIF cage, and PEEK cage alone. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone.
In addition, the bone-formation ability of these corticocancellous chips is similar to ICBG, which had been shown by Miura et al31 and Carragee et al.32 The configurations of ABIF cages were made in accordance with similar PEEK cage configurations. Cho et al33 had provided guidelines on the appropriate geometry of intervertebral spacers, including shape, length, and surface profile, so as to maximize construct stability when the cages are used in conjunction with posterior fixation. Following these recommendations, designs of ABIF cage consist of a solid hexahedron with biconvex surfaces, which is made to fit the concave shape of superior and inferior endplates. The serrated surfaces of cage can help stabilize the implant position to avoid migration.
Biomechanical Stability of ABIF Cage The aim of this study was to evaluate biomechanical characteristics of ABIF cage compared with ICBG and PEEK cage in single segment. With ICBG alone or cage alone, ROM in lateral bending was slightly greater than that in intact level, although this was not statistically significant. This is similar to results reported by Lund et al,34 who revealed that standalone cages inserted posteriorly could not significantly stabilize the spinal segment, especially in extension and rotation. In addition, several previous studies emphasize the importance of posterior disc material and posterior annulus in stability in flexion,35 both of which are removed to allow insertion of posterior interbody cages. Regarding comparison of 3 intervertebral spacers used in current study, the stability provided by PEEK cage alone was found to slightly exceed that of ICBG and ABIF cage in all directions, although this difference was not statistically significant. Also, no statistically significant difference in ROM was observed once the cage or bone graft supplemented with posterior instrumentation. The ROM in all directions showed statistically significant improvement in stability compared with cages alone, which is in agreement with previous studies.36 Furthermore, several authors37,38 recommend that posterior fixation in lumbar vertebrae should E690
Biomechanical Evaluation; a Novel Cage • Wang et al
be performed with posterior instrumentation. Supplementation with posterior fixation has been shown to result in fusion rates approaching 98.9%,22 largely due to additional stability afforded by pedicle screw and rod construction. In addition, as ABIF cages made of autogenous bone have the properties consistent with the bone graft surface, the high local stress on cutting through vertebral body may be avoided and it may provide a good foundation for integration. The failure load was another parameter used to evaluate stiffness of ABIF cage. Previously, An et al39 found that the BMD of the graft showed a significant correlation with load to failure. To test the mechanical properties of the ABIF cage in the similar condition, we used the same amount of bone chips to prefabricate the same volume of ABIF cages. Actually, the failure load of ABIF cage with a mean BMD of 0.58 g/cm2 is 3.25 kN and is slightly higher than that of ICBG with a mean BMD of 0.54 g/cm2. However, failure load of PEEK cages is 6.83 kN and makes a split fracture in vertebral body when failing. Ideal failure load of cages should probably be able to withstand supraphysiological load in order to prevent failure. Wilke et al40 measured intradiscal pressure in vivo in L4–L5 spinal motion segment in humans and found intradiscal pressure depended on the type of preceding activity, posture, external loads, and muscular activity. Kandziora et al41 converted intradiscal pressure to load and in L4–L5 motion segment of a patient weighing 80 kg found peak loads on the order of 2.24 kN. Therefore, although failure load of PEEK cages was higher than in ICBG or ABIF, failure load of all cages tested was higher than this in vivo peak load measure, suggesting that all tested cages meet the threshold to adequately perform clinically during the long term. In our study, several factors could limit the extent to which the results can be generalized. First, the result of this test reflected only short-term stability, with relatively few loading cycles to project longer-term biomechanical efficacy. Second, our study described the acute biomechanical features of ABIF cages in vitro, and their performances in vivo are unknown. Furthermore, we should also compare the clinical efficacy between the ABIF cage and the morselized bone chips with merely an equal volume in the future clinical study. Third, as surrounding muscles of spine are important parameters to evaluate biomechanical characteristics in spinal fusion,42 current testing was not able to retain all endogenous structures. Fourth, as we did not measure the pressure of ABIF cage preparation that can vary from one surgeon to another, in the future, this pressure should be measured for consistency. Fifth, often fusion procedures were done in patients with low BMD and/or with degenerated spine. Therefore, the detail of clinical data will be summarized and showed at the follow-up in later study.
CONCLUSION The current study showed that ABIF cage alone can provide appropriate stiffness at the physiological loads. In addition, ROM and stiffness of ABIF cages with pedicle screw fixation system are similar to that of PEEK cages with posterior
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BIOMECHANICS instrumentation. ABIF cages also have the inherent properties of osteoconduction and osteoinduction. Therefore, ABIF cages have the appropriate mechanical strength compared with current interbody cages and theoretically retain adequate biological activity.
➢ Key Points Traditional synthetic interbody spacers or corticocancellous ICBG using in PLIF has demonstrated drawbacks including subsidence of metallic cages and donor site morbidity. A novel ABIF cage is prefabricated by morselized small corticocancellous chips. The ABIF cage without supplemental fixation was able to decrease ROM and NZ to near intact levels as well as the ICBG, PEEK cage. When stabilized with pedicle screws, the ABIF cage is biomechanically as stable as ICBG cage and PEEK cage with posterior instrumentation. Although the failure load of PEEK cage was the highest in the axial compression testing, there is no significant difference between the ICBG cage and the ABIF cage.
References
1. Jaslow LA. Intercorporal bone graft in spinal fusion after disc removal. Surg Gynecol Obstet 1946;82:215–8. 2. Cloward RB. The treatment of ruptured lumbar intervertebral discs by vertebral body fusion. J Neurosurg 1953;10:154–68. 3. Cloward RB. Posterior lumbar interbody fusion update. Clin Orthop 1985;193:16–9. 4. Bagby GW. Arthrodesis by the distraction-compression method using a stainless steel implant. Orthopedics 1988;11:931–4. 5. Beutler WJ, Peppelman WC Jr. Anterior lumbar fusion with paired BAK standard and paired BAK proximity cages: subsidence incidence, subsidence factors, and clinical outcome. Spine J 2003;3:289–93. 6. Lazennec JY, Madi A, Rousseau MA, et al. Evaluation of the 96/4 PLDLLA polymer resorbable lumbar interbody cage in a long term animal model. Eur Spine J 2006;15:1545–53. 7. Elias JE, Simmons NE, Kaptain GJ, et al. Complication of posterior lumbar interbody fusion when using a titanium thread cage device. J Neurosurg 2000;93:45–52. 8. Jockisch KA, Brown SA, Bauer TW, et al. Biological response to chopped carbon fiber reinforced PEEK. J Biomed Master Res 1992;26:133–46. 9. Ahlmann E, Patzakis M, Roidis N, et al. Comparison of anterior and posterior iliac crest bone grafts in terms of harvest-site morbidity and functional outcomes. J Bone Joint Surg Am 2002;84-A: 716–20. 10. Sasso RC, LeHuec JC, Shaffrey C, et al. Iliac crest bone graft donor site pain after anterior lumbar interbody fusion: a prospective patient satisfaction outcome assessment. J Spinal Disord Tech 2005;18(suppl):S77–81. 11. Simmons JW. Posterior lumbar interbody fusion with posterior elements as chip grafts. Clin Orthop Relat Res 1985;(193):85–9. 12. Turner JA, Ersek M, Herron L, et al. Patient outcomes after lumbar spinal fusions. JAMA 1992;268:907–11. 13. Enker P, Steffee AD. Interbody fusion and instrumentation. Clin Orthop 1994;300:90–101.
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14. Lam FC, Alkalay R, Groff MW. The effects of design and positioning of carbon fiber lumbar interbody cages and their subsidence in vertebral bodies. J Spinal Disord Tech 2012;25:116–22. 15. Cripton PA, Bruehlmann SB, Orr TE, et al. In vitro axial preload application during spine flexibility testing: towards reduced apparatus-related artefacts. J Biomech 2000;33:1559–68. 16. Vadapalli S, Robon M, Biyani A, et al. Effect of lumbar interbody cage geometry on construct stability: a cadaveric study. Spine 2006;31:2189–94. 17. Cheng BC, Gorden J, Cheng J, et al. Immediate biomechanical effects of lumbar posterior dynamic stabilization above a circumferential fusion. Spine 2007;32:2551–7. 18. 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;7:148–54. 19. Steffen T, Tsantrizos A, Aebi M. Effect of implant design and endplate preparation on the compressive strength of interbody fusion constructs. Spine (Phila Pa 1976) 2000;25:1077–84. 20. Brantigan JW, Steffee AD, Geiger JM. A carbon fibre implant to aid interbody lumbar fusion. Spine 1991;16(suppl):S277–82. 21. Brantigan JW, Steffee AD, Lewis ML, et al. Lumbar interbody fusion using the Brantigan I/F cage for posterior lumbar interbody fusion and the variable pedicle screw placement system: two-year results from a Food and Drug Administration investigational device exemption clinical trial. Spine 2000;25:1437–46. 22. Jenis LG, Banco RJ, Kwon B. A prospective study of Autologous Growth Factors (AGF) in lumbar interbody fusion. Spine J 2006;6:14–20. 23. Goulet J, Senunas L, DeSilva G, et al. Autogenous iliac crest bone graft: complications and functional assessment. Clin Orthop Relat Res 1997;339:76–81. 24. Heary R, Schlenk R, Sacchieri T, et al. Persistent iliac crest donor site pain: independent outcomes assessment. Neurosurgery 2002;50:510–6. 25. Bezer M, Kocaog˘ lu B, Aydin N, et al. Comparison of traditional and intrafascial iliac crest bone-graft harvesting in lumbar spinal surgery. Int Orthop 2004;28:325–8. 26. Arrington ED, Smith WJ, Chambers HG, et al. Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res 1996;(329): 300–9. 27. Vadapalli S, Sairyo K, Goel VK, et al. Biomechanical rationale for using polyetheretherketone (PEEK) spacers for lumbar interbody fusion—a finite element study. Spine (Phila Pa 1976) 2006;31:E992–8. 28. Kim YH, Choi DK, Kim K. Investigation of the compressive stiffness of spinal cages in various experimental conditions based on finite element analysis. Proc Inst Mech Eng H 2012;226:341–4. 29. Togawa D, Bauer TW, Lieberman IH, et al. Lumbar intervertebral body fusion cages: histological evaluation of clinically failed cages retrieved from humans. J Bone Joint Surg Am 2004;86-A:70–9. 30. Gloria A, Manto L, De Santis R, et al. Biomechanical behavior of a novel composite intervertebral body fusion device. J Appl Biomater Biomech 2008;6:163–9. 31. Miura Y, Imagama S, Yoda M, et al. Is local bone viable as a source of bone graft in posterior lumbar interbody fusion? Spine 2003;28:2386–9. 32. Carragee EJ, Comer GC, Smith MW. Local bone graft harvesting and volumes in posterolateral lumbar fusion: a technical report. Spine J 2011;11:540–4. 33. Cho W, Wu C, Mehbod AA, et al. Comparison of cage designs for transforaminal lumbar interbody fusion: a biomechanical study. Clin Biomech (Bristol, Avon) 2008;23:979–85. 34. Lund T, Oxland TR, Jost B, et al. Interbody cage stabilisation in the lumbar spine: biomechanical evaluation of cage design, posterior instrumentation and bone density. J Bone Joint Surg Br 1998;80:351–9. 35. Goel VK, Nishiyama K, Weinstein JN, et al. Mechanical properties of lumbar spinal motion segments as affected by partial disc removal. Spine 1986;11:1008–12. 36. Oxland TR, Lund T. Biomechanics of stand-alone cages and cages in combination with posterior fixation: a literature review. Eur Spine J 2000;9(suppl 1):S95–101. www.spinejournal.com
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BIOMECHANICS 37. Glazer PA, Colliou O, Klisch SM, et al. Biomechanical analysis of multilevel fixation methods in the lumbar spine. Spine 1997;22:171–82. 38. Rathonyi GC, Oxland TR, Gerich U, et al. The role of supplemental translaminar screws in anterior lumbar interbody fixation: a biomechanical study. Eur Spine J 1998;7: 667–79. 39. An HS, Xu R, Lim TH, et al. Prediction of bone graft strength using dual-energy radiographic absorptiometry. Spine (Phila Pa 1976) 1994;19:2358–62; discussion 2362–3.
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40. Wilke H, Neef P, Hinz B, et al. Intradiscal pressure together with anthropometric data—a data set for the validation of models. Clin Biomech (Bristol, Avon) 2001;16(suppl 1):S111–26. 41. Kandziora F, Pflugmacher R, Kleemann R, et al. Biomechanical analysis of biodegradable interbody fusion cages augmented With poly(propylene glycol-co-fumaric acid). Spine (Phila Pa 1976) 2002; 27:1644–51. 42. Goel VK, Panjabi MM, Patwardhan AG, et al. Test protocols for evaluation of spinal implants. J Bone Joint Surg Am 2006;88 (suppl 2):103–9.
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Biomechanical Evaluation of a Novel Autogenous Bone Interbody Fusion Cage for Posterior Lumbar Interbody Fusion in a Cadaveric Model Le Wang, MS,* Kyle T. Malone, MS,† Hai Huang, MS,* Zhenshan Zhang, MS,* Zhi Zhang, MD,* Liang Zhang, MD,* and Jian Li, MD, PhD*
Study Design. A human cadaveric biomechanical study of a novel, prefabricated autogenous bone interbody fusion (ABIF) cage. Objective. To evaluate the biomechanical properties of the ABIF cage in a single-level construct with and without transpedicular screw and rod fixation. Summary of Background Data. In current practice, posterior lumbar interbody fusion is generally carried out using synthetic interbody spacers or corticocancellous iliac crest bone graft (ICBG) in combination with posterior instrumentation. However, questions remain concerning the use of synthetic intervertebral implants as well as the morbidity ICBG harvesting. Therefore, ABIF cage has been developed to obviate some of the challenges in conventional posterior lumbar interbody fusion instrumentation and to facilitate the fusion process. Methods. Eighteen adult cadaveric lumbosacral (L3–S1) specimens were tested. Test conditions included single lumbosacral segments across (1) intact, (2) decompressed, (3) intervertebral cage alone, and (4) intervertebral cage with bilateral transpedicular fixation. Range of motion (ROM), neutral zone (NZ), and axial failure load were tested for each condition. Results. The ICBG, polyetheretherketone cage, or ABIF cage alone exhibited a significantly lower (P < 0.05) ROM and NZ than the decompressed spine. In comparison with the intact spine, all 3 test conditions without supplemental fixation were able to decrease ROM and NZ to near intact levels. When stabilized with pedicle screws, the ROM was significantly less and the NZ was significantly From the *Institute of Orthopaedics and Traumatology, the Third Affiliated Hospital, Guangzhou Medical University, People’s Republic of China; and †NNI Research Foundation, Las Vegas, NV. Acknowledgment date: September 18, 2013. First revision date: January 13, 2014. Second revision date: February 9, 2014. Acceptance date: February 12, 2014. The device(s)/drug(s) that is/are the subject of this manuscript is/are not FDA approved for this indication and is/are not commercially available in the United States. National Natural Science Foundation of China (No.31200726) grant funds were received to support this work. Relevant financial activities outside the submitted work: grant. Address correspondence and reprint requests to Jian Li, MD, PhD, Institute of Orthopaedics and Traumatology, the Third Affiliated Hospital, Guangzhou Medical University, 63, Duobao Rd, Guangzhou, 510150, People’s Republic of China; E-mail: [email protected] DOI: 10.1097/BRS.0000000000000291
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lower (P < 0.05) for each group both compared with the intact spine. In axial compression testing, the failure load of polyetheretherketone cage was the highest, with no significant difference between the ICBG and the ABIF cage. Conclusion. These data suggest that the novel ABIF cage can bear the physiological intervertebral peak load, similar to ICBG. When combined with pedicle screw and rod fixation, it exhibits similar biomechanical properties as the polyetheretherketone cage plus posterior instrumentation. Based on the biomechanical properties of ABIF cage, the prospect of these cages in clinical practice is expected. Key words: posterior lumbar interbody fusion, autogenous bone, cage, pedicle screws. Level of Evidence: N/A Spine 2014;39:E684–E692
P
osterior lumbar interbody fusion (PLIF) is a wellestablished surgical procedure in treatment of a variety of lumbar degenerative conditions since its introduction by Jaslow1 and subsequent modification by Cloward.2,3 The surgical goals of PLIF are to provide a solid fusion with direct neural decompression, to restore normal disc height, realign spinal segment, and provide an adequate fusion environment, thereby hastening postoperative rehabilitation and fusion process.4 In general, PLIF is performed using synthetic intervertebral cages with autogenous bone, corticocancellous iliac crest bone graft (ICBG), or other bone graft material implanted in the intervertebral space. However, previous studies have reported several complications in the use of synthetic cages, including risk for subsidence and corrosive effects, which have recently been noted to contribute to an increasing incidence of revision surgery.5,6 In addition, cages still require bone graft material and do not incorporate as part of the fusion mass, which may create immunological problems.7,8 Moreover, harvesting autologous bone graft from iliac crest is associated with a significant morbidity that can occur in as many as 30% to 40% of patients.9,10 In an effort to resolve such problems of mechanical cage devices and morbidity of ICBG, Simmons11 developed the concept of harvesting corticocancellous autologous bone from the posterior elements of vertebra being treated itself.
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BIOMECHANICS When spinal cord was decompressed, the lamina and spinous process were cut into small corticocancellous chips and subsequently used as graft material. These corticocancellous chips were used to fill in the intervertebral space for facilitation of fusion. In a retrospective study, Turner et al12 found that PLIF with such corticocancellous chips provided the highest fusion rate and the most satisfactory clinical results. However, some problems such as collapse and pseudarthrosis have been reported when these bone grafts were used.13 Furthermore, one of the major problems is that such bone graft cannot provide sufficient mechanical strength compared with ICBG or synthetic cages. To avoid the collapse of these bone grafts and to satisfy the biological requirements of spinal fusion, a machine designed to compress and prefabricate a novel cage consisting of morselized autogenous bone was developed by the authors of current study. This implant has been designated as an autogenous bone interbody fusion (ABIF) cage. As ABIF cage is a novel implant, no biomechanical or testing has been published to compare its mechanical properties with alternative cages. The purpose of this study was to analyze the axial compression properties of ABIF cage and to evaluate the biomechanical characteristics of this novel cage in comparison with ICBG and polyetheretherketone (PEEK) cages in a single-level of lumbar spine.
MATERIALS AND METHODS Specimen Preparation Eighteen fresh-frozen L3–S1 spine segments and ICBGs were obtained from the department of Pathology, Guangzhou Medical University, for use in the current biomechanical testing. Mean specimens’ age was 50 years (standard deviation: 8.9 yr, range: 35–65 yr) and were made up of 7 males and 11 females. Ethics committee approval for use of the specimens was granted by the ethics committee of Guangzhou Medical University. All specimens were radiographed for any abnormalities or spinal fractures. As bone quality is always a concern in such laboratory testing,14 dual-energy x-ray absorptiometry was performed in anterior posterior direction to measure the bone mineral density (BMD) of each vertebra. The spinal segments were stored in a freezer at −20°C. Before testing, the spine was thawed and kept moistened with saline. The L3–S1 segments were used in all range of motion (ROM)
Biomechanical Evaluation; a Novel Cage • Wang et al
and neutral zone testing, although the L4–L5 level was the only level treated. In addition, the L4–L5 was a separate functional spinal unit in the axial compression test.
ABIF Cage Preparation ABIF cage is fabricated in 2 steps. The first step involves preparation of raw materials. When spinal cord is decompressed during the PLIF procedure, the lamina and spinous process are cut into small corticocancellous chips measuring 2 to 4 mm (Figure 1A–D). The second step involves placement of these harvested local corticocancellous chips into a cageshaped groove at the bottom of a specialized machine (China Pat. No. ZL201120261348.8), which can generate enough vertical pressure by twisting a rotatable handle and compact the corticocancellous chips into ABIF cage. Preparation of an ABIF cage took 3.0 g corticocancellous chips, which was measured by electronic balance. The configuration of this cage was followed the design of standard PEEK cage (Wego Holding Co Limited, Weihai, China), and the implant dimensions were 16 × 6 × 13 mm (length × height × width). The configurations of ABIF cage, PEEK cage, and ICBG are showed in Figure 2. In addition, the BMD of the ABIF cages and the ICBG were measured by dual-energy x-ray absorptiometry as a reference.
Testing
Each L3–S1 specimen (n = 18) served as its own control and was tested in the following sequence (Figure 3): (1) intact (control group, n = 18) and (2) decompressed (post L4–L5 laminectomy, including medial facetectomy involving 50% of the facet joint and resection of the posterior longitudinal ligaments, n = 18). After testing on conditions 1 and 2, all specimens were randomly assigned to one of the following test conditions for evaluation of interbody cage stiffness using ICBG (n = 6), PEEK cage (n = 6), or ABIF cage (n = 6) at L4-–L5. After interbody cage stiffness testing, each L4–L5 segment within L3–S1 construct was additionally stabilized with pedicle screws (Wego Holding Co Limited, Weihai, China) (each group, n = 6). To ensure consistency in the procedure performed between specimens, a single surgeon performed all decompression and PLIF procedures. In addition, the failure loads of ICBGs, ABIF cages, and PEEK cages were evaluated in L4–L5 segments alone through an axial compression test (each group, n = 6).
Figure 1. A series of images showing the process of autogenous bone interbody fusion (ABIF) cage preparation. Small corticocancellous bones were obtained from the posterior decompression performed prior to posterior lumbar interbody fusion (A). Using a specialized compressive machine (China Pat. No. ZL 2011 2 0261348.8 [21 Mar 2012]), the raw materials were prefabricated into the ABIF cage (B and C). Images showing the ABIF cage (D). Spine
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Figure 2. Superior and lateral views of iliac crest bone graft (A). Images showing the dimensions of the autogenous bone interbody fusion cage (B). Superior and lateral views of a polyetheretherketone cage (C).
Stiffness Testing The L3 and S1 vertebrae were set in polymethylmethacrylate. Each specimen was placed in a spinal loading frame capable of applying independent bending moments and axial loads (MTS 858, MTS Systems, Eden Prairie, MN) (Figure 4). The spine simulator consisted of an axial torsion actuator and 2 rotational actuators for lateral bending and flexion– extension. These actuators were mounted on the upper side of the test machine. A low-friction cross roller slide table mounted on the lower side allowed pure bending moments to be applied to the specimen. After fixing the spine to an immobile base plate within the testing frame, labeled steel pins with
infrared light emitting diodes were attached to L4 and L5 vertebrae. A special set of light emitting diodes was also attached to the immobile base for reference. The 3-dimensional locations of the light emitting diodes were quantified after each loading step by a motion analysis system (VICON; Oxford Metrics, Ltd., Oxford, United Kingdom), and 3 images were obtained during each test cycle. A 100 N axial compressive preload was maintained throughout each test so as not to damage the specimens that lacked musculature and joint support, and this small preload was used in an effort to minimize the amount of artifact.15 After specimen was mounted on the spinal tester, left–right
Eighteen fresh-frozen L3–S1 spine segments in humans
(1) Intact state (n = 18)
(2) Decompressed state (n = 18)
ROM and stiffness test
(3) Autologous iliac crest bone
(4) ABIF cage
(4) PEEK cage
graft alone (n = 6)
alone (n = 6)
alone (n = 6)
(6) Iliac crest bone graft or cage combined with pedicle screws fixation (n = 6, each group)
Axial compression test
Autologous iliac crest bone graft alone (n = 6)
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ABIF cage alone
PEEK cage alone
(n = 6)
(n = 6)
Figure 3. The testing sequence of the three grafts. ROM indicates range of motion; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone
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expressed as mean ± SD. Comparison of ROM, NZ, stiffness, and failure load was performed using 1-way analysis of variance for independent samples, followed by a StudentNeumann-Keuls-q test for multiple comparisons.
RESULTS
Average BMD and T and Z scores of specimens were 1.05 ± 0.14 g/cm2, 0.44 ± 0.61, and 1.16 ± 0.69, respectively. These parameters showed nearly normal values. In addition, the BMD of the ABIF cage was reached from 0.52 to 0.62 g/cm2, with a mean of 0.58 g/cm2, and that of the ICBG was reached from 0.48 to 0.59 g/cm2, with a mean of 0.54 g/cm2. There were no statistically significant differences in BMD between these 2 grafts (P > 0.05).
ROM and Stiffness Figure 4. Image showing laboratory testing setup.
lateral bending, flexion–extension, and left–right axial rotation of the specimen with a maximum moment loads of ±6 N·m16,17 were conducted at a constant speed of 0.5° per second in sequence before and after different surgical procedures. The order of directional sequences for loading was randomized. Three cycles were applied for each loading condition, with the last cycle used for data analysis. After each test mode, the specimens were allowed to relax for 60 seconds before further data were recorded. The ROM, neutral zone (NZ), elastic zone, and the stiffness values were calculated from the corresponding load-displacement curves. In brief, the ROM was calculated between an applied load of 6 N·m and −6 N·m. The NZ was defined as the difference in angulation at load of 0 N·m between the 2 phases of motion. The elastic zone was defined from the end of the NZ to the point of the maximal loading. Stiffness in elastic zone was estimated as the inverse slope of a trend line applied to the load displacement curve at ±6 N·m. For further analysis, values were averaged over both movement directions.18
Axial Compression Test of ABIF Cage After stiffness testing, the PEEK cages, ABIF cages, and ICBG were tested in compression with the same machine. For this test, L4 and L5 vertebral bodies were potted using polymethylmethacrylate and constrained from rotation during the test. Axial compression displacement was applied at the constant speed of 5 mm/min. While applying loading, compressive force and displacement data were recorded with 25 Hz. The real-time compressive load displacement curve was electronically recorded. Finally, the compression test was continued until failure as evidenced by a drop or a split fracture in vertebral body or in the construct. The failure load was defined as the point at which further deformation resulted in a decrease of measured force.19
Data and Statistical Analysis All data were analyzed using SPSS software, and statistically significant values were defined as P < 0.05. The data were Spine
Compared with intact spine and all subsequent test conditions, the mean ROM of decompressed state was statistically significantly higher (P < 0.05), especially in flexion–extension. In comparison with decompressed state, the addition of ICBG, PEEK cage, or ABIF cage alone was able to reduce ROM and NZ to near intact levels (P < 0.05). Meanwhile, the mean angular displacement value in lateral bending was still slightly greater than intact spine but was not statistically significant. The ROM and NZ of PEEK cage alone group were slightly lower than those of ICBG or ABIF cage alone group. However, the difference was not statistically significant. This meant that no single cage or bone graft was statistically different from any of the others. Intuitively, compared with the cage or bone graft alone groups, the groups stabilized with posterior pedicle screws demonstrated a significantly lower (P < 0.05) ROM and NZ in all planes of motion. In addition, there were no statistically significant differences in ROM of NZ between groups (ABIF, PEEK, or ICBG stabilized with pedicle screws [P > 0.05]) (Table 1). The stiffness data of each group were normalized to the intact state. Compared with the stiffness of intact state, the values in decompressed state were decreased in all testing conditions. In addition, there was no significant difference among ICBG, PEEK cage, and ABIF cage alone groups in all directions. Furthermore, each experimental group stabilized with pedicle screws showed significantly higher stiffness (P < 0.05) than the single cage or bone graft group (Table 2) (Figure 5).
Axial Compression Testing The real-time compressive load displacement curve for the 3 grafts was showed in Figure 6. In comparison with ICBG and ABIF groups, the failure load was significantly higher in PEEK cage group (6.83 ± 0.92 kN) (P < 0.05). In addition, all specimens exhibited a split fracture in vertebral body when using PEEK cage alone. However, as shown in Figure 7, ICBG and ABIF cage collapsed and fractured when axial compression was added. In addition, the failure load of ABIF cage (3.25 ± 0.39 kN) was slightly higher than ICBG group (2. 96 ± 0.25 kN), although there was no observed statistical difference (Table 3) (Figure 8). www.spinejournal.com
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1.15 ± 0.05
1.61 ± 0.25*
1.21 ± 0.09*†
5.36 ± 0.31*†
3.45 ± 0.65†
10.91 ± 1.52†
4.31 ± 0.47*†
14.66 ± 1.32*†
ICBF Alone
1.18 ± 0.08*†
5.30 ± 0.38*†
3.44 ± 0.58†
10.87 ± 1.64†
4.21 ± 0.50*†
14.44 ± 1.60*†
ABIF Cage Alone
1.24 ± 0.07*†
5.18 ± 0.45*†
3.35 ± 0.61†
10.75 ± 1.65†
4.25 ± 0.45*†
14.25 ± 1.25*†
PEEK Cage Alone
0.15 ± 0.02*†‡
1.21 ± 0.14*†‡
0.91 ± 0.04*†‡
2.11 ± 0.71*†‡
0.51 ± 0.08*†‡
2.91 ± 0.02*†‡
ICBF + PPSFS
0.11 ± 0.03*†‡
0.91 ± 0.05*†‡
0.83 ± 0.08*†‡
2.01 ± 0.68*†‡
0.48 ± 0.03*†‡
2.79 ± 0.06*†‡
ABIF Cage + PPSFS
0.10 ± 0.01*†‡
0.98 ± 0.09*†‡
0.82 ± 0.05*†‡
1.97 ± 0.75*†‡
0.45 ± 0.06*†‡
2.74 ± 0.05*†‡
PEEK Cage + PPSFS
2.93 ± 0.38 100 ± 13.05 5.85 ± 0.59 100 ± 10.12
Bending (N·m/degree)
Normalized (%)
Rotation (N·m/degree)
Normalized (%) 43.55 ± 10.56
2.55 ± 0.62
53.41 ± 9.21
1.56 ± 0.27
48.52 ± 12.52
1.17 ± 0.31
Decompressed
1.87 ± 0.28
ABIF Cage
2.67 ± 0.30
2.79 ± 0.43
79.60 ± 8.51
1.95 ± 0.21
PEEK Cage
5.67 ± 0.51
ABIF Cage + PPSFS
6.50 ± 0.69
6.54 ± 0.65
223.91 ± 21.04 231.44 ± 20.87
5.49 ± 0.52
ICBF + PPSFS
79.41 ± 8.02
4.65 ± 0.47
79.01 ± 7.10
4.62 ± 0.42
82.77 ± 8.11
4.84 ± 0.47
8.62 ± 0.94 145.55 ± 20.11 147.41 ± 16.12
8.51 ± 1.18
90.11 ± 11.12 91.21 ± 10.37 95.14 ± 14.84 221.95 ± 23.54 223.12 ± 22.32
2.64 ± 0.33
74.11 ± 10.41 76.51 ± 11.60
1.82 ± 0.26
ICBF
*For statistical evaluation, see text. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone; PPSFS, posterior pedicle screw fixation system.
100 ± 12.05
2.45 ± 0.31
Intact
Normalized (%)
Flexion–extension (N·m/degree)
Conditions Directions
148.24 ± 18.31
8.67 ± 1.07
234.15 ± 19.18
6.86 ± 0.56
233.04 ± 21.12
5.71 ± 0.52
PEEK Cage + PPSFS
TABLE 2. Stiffness (N·m/Degree) in the EZ of the 3 Grafts Tested in the Study in Response to Different Conditions and Directions*
*Significant difference in comparison with intact motion segment. †Significant difference in comparison with decompressed motion segment. ‡Significant difference in comparison with the cage or ICBF alone. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone; PPSFS, posterior pedicle screw fixation system; ROM, range of motion; NZ, neutral zone.
NZ
6.92 ± 1.09*
4.51 ± 0.95*
3.21 ± 0.68
4.21 ± 0.42
14.61 ± 1.58*
ROM
Rotation
NZ
ROM
5.58 ± 0.54*
19.05 ± 1.97*
Decompressed
10.31 ± 1.35
3.64 ± 0.52
NZ
Bending
12.20 ± 1.62
Intact
ROM
Flexion–extension
Test Mode (°)
extension, Rotation (Both Sides), and Bending (Both Sides) (χ ± s°)
TABLE 1. Range of Motion, Neutral Zone of the Different Bone Graft, or Cages Tested in the Study in Response to Flexion-
BIOMECHANICS Biomechanical Evaluation; a Novel Cage • Wang et al
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Biomechanical Evaluation; a Novel Cage • Wang et al
Figure 7. Images showing the iliac crest bone graft (A) and the autogenous bone interbody fusion cage (B) collapsed and fractured after axial compression testing. Figure 5. Graph of the stiffness results normalized to the intact motion segment in the elastic zone. *Significant difference in comparison with intact motion segment. †Significant difference in comparison with decompressed motion segment. ‡Significant difference in comparison to the cage or ICBF alone. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone.
DISCUSSION Design of ABIF Cage Rigid spinal stabilization using intervertebral cages or bone grafts with transpedicular screw instrumentation has resulted in increased fusion rates with superior clinical outcomes compared with those without supplemental internal fixation.20,21 In addition to the biomechanical properties of intervertebral spacers, their biological properties (or lack thereof) additionally factor into the final fusion construct. Autograft has significant advantages and is considered the “gold standard” for bone graft material in fusion procedures because of its inherent properties of osteoconduction, osteoinduction, and provision of a cellular component for bone healing.22 However, graft site complications and morbidity are not uncommon in harvesting autograft, including wound infection, hematoma, iliac crest fracture, and donor site pain.23–26 The variable
Figure 6. The typical load displacement curve of the 3 grafts in axial compression testing. Black arrows represent change in slope from positive to negative, indicating the failure load of each graft. PEEK indicates polyetheretherketone; ABIF, autogenous bone interbody fusion; ICBF, iliac crest bone graft. Spine
incidence of complications in using autologous bone has led to the development of synthetic intervertebral implants. Currently, although cages made of PEEK claim advantage in that its Young modulus (“E” = 3.6–4 GPa) is similar to that of cortical bone (“E” = 12 GPa),27,28 the difference still remains. Cages manufactured using medical alloys do not have the ability to promote bone ingrowth, and the cage material does not exhibit degradation in vivo.29,30 To reduce the incidence of complications in using autologous ICBG and to overcome the disadvantages of alloy cages described previously, this study evaluated implants developed using a machine to compress small corticocancellous chips, previously considered waste, to prefabricate an ABIF cage.
TABLE 3. The Demographics, BMD, and Failure
Load of Each Specimen
No.
Sex Age (yr) BMD (g/cm2) Failure Load (kN)
1. ABIF
F
45
1.09
3.10
2. ABIF
F
63
1.12
3.78
3. ABIF
F
56
0.68
2.90
4. ABIF
M
50
1.00
2.82
5. ABIF
M
58
1.08
3.63
6. ABIF
F
65
1.07
3.27
7. ICBG
F
48
1.17
3.12
8. ICBG
M
35
0.83
2.77
9. ICBG
F
45
1.03
2.67
10. ICBG
M
64
1.09
2.88
11. ICBG
M
47
1.11
2.93
12. ICBG
F
36
1.25
3.37
13. PEEK
F
46
0.89
6.29
14. PEEK
F
52
1.13
6.85
15. PEEK
M
39
1.08
7.95
16. PEEK
F
45
1.06
6.62
17. PEEK
M
54
1.26
7.76
18. PEEK
F
48
1.03
5.51
BMD indicates bone mineral density; ABIF, autogenous bone interbody fusion; F, female; M, male; ICBG, iliac crest bone graft; PEEK, polyetheretherketone.
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BIOMECHANICS
Figure 8. Graph showing the results of axial compression testing of the ICBF, ABIF cage, and PEEK cage alone. ICBF indicates iliac crest bone graft; ABIF, autogenous bone interbody fusion; PEEK, polyetheretherketone.
In addition, the bone-formation ability of these corticocancellous chips is similar to ICBG, which had been shown by Miura et al31 and Carragee et al.32 The configurations of ABIF cages were made in accordance with similar PEEK cage configurations. Cho et al33 had provided guidelines on the appropriate geometry of intervertebral spacers, including shape, length, and surface profile, so as to maximize construct stability when the cages are used in conjunction with posterior fixation. Following these recommendations, designs of ABIF cage consist of a solid hexahedron with biconvex surfaces, which is made to fit the concave shape of superior and inferior endplates. The serrated surfaces of cage can help stabilize the implant position to avoid migration.
Biomechanical Stability of ABIF Cage The aim of this study was to evaluate biomechanical characteristics of ABIF cage compared with ICBG and PEEK cage in single segment. With ICBG alone or cage alone, ROM in lateral bending was slightly greater than that in intact level, although this was not statistically significant. This is similar to results reported by Lund et al,34 who revealed that standalone cages inserted posteriorly could not significantly stabilize the spinal segment, especially in extension and rotation. In addition, several previous studies emphasize the importance of posterior disc material and posterior annulus in stability in flexion,35 both of which are removed to allow insertion of posterior interbody cages. Regarding comparison of 3 intervertebral spacers used in current study, the stability provided by PEEK cage alone was found to slightly exceed that of ICBG and ABIF cage in all directions, although this difference was not statistically significant. Also, no statistically significant difference in ROM was observed once the cage or bone graft supplemented with posterior instrumentation. The ROM in all directions showed statistically significant improvement in stability compared with cages alone, which is in agreement with previous studies.36 Furthermore, several authors37,38 recommend that posterior fixation in lumbar vertebrae should E690
Biomechanical Evaluation; a Novel Cage • Wang et al
be performed with posterior instrumentation. Supplementation with posterior fixation has been shown to result in fusion rates approaching 98.9%,22 largely due to additional stability afforded by pedicle screw and rod construction. In addition, as ABIF cages made of autogenous bone have the properties consistent with the bone graft surface, the high local stress on cutting through vertebral body may be avoided and it may provide a good foundation for integration. The failure load was another parameter used to evaluate stiffness of ABIF cage. Previously, An et al39 found that the BMD of the graft showed a significant correlation with load to failure. To test the mechanical properties of the ABIF cage in the similar condition, we used the same amount of bone chips to prefabricate the same volume of ABIF cages. Actually, the failure load of ABIF cage with a mean BMD of 0.58 g/cm2 is 3.25 kN and is slightly higher than that of ICBG with a mean BMD of 0.54 g/cm2. However, failure load of PEEK cages is 6.83 kN and makes a split fracture in vertebral body when failing. Ideal failure load of cages should probably be able to withstand supraphysiological load in order to prevent failure. Wilke et al40 measured intradiscal pressure in vivo in L4–L5 spinal motion segment in humans and found intradiscal pressure depended on the type of preceding activity, posture, external loads, and muscular activity. Kandziora et al41 converted intradiscal pressure to load and in L4–L5 motion segment of a patient weighing 80 kg found peak loads on the order of 2.24 kN. Therefore, although failure load of PEEK cages was higher than in ICBG or ABIF, failure load of all cages tested was higher than this in vivo peak load measure, suggesting that all tested cages meet the threshold to adequately perform clinically during the long term. In our study, several factors could limit the extent to which the results can be generalized. First, the result of this test reflected only short-term stability, with relatively few loading cycles to project longer-term biomechanical efficacy. Second, our study described the acute biomechanical features of ABIF cages in vitro, and their performances in vivo are unknown. Furthermore, we should also compare the clinical efficacy between the ABIF cage and the morselized bone chips with merely an equal volume in the future clinical study. Third, as surrounding muscles of spine are important parameters to evaluate biomechanical characteristics in spinal fusion,42 current testing was not able to retain all endogenous structures. Fourth, as we did not measure the pressure of ABIF cage preparation that can vary from one surgeon to another, in the future, this pressure should be measured for consistency. Fifth, often fusion procedures were done in patients with low BMD and/or with degenerated spine. Therefore, the detail of clinical data will be summarized and showed at the follow-up in later study.
CONCLUSION The current study showed that ABIF cage alone can provide appropriate stiffness at the physiological loads. In addition, ROM and stiffness of ABIF cages with pedicle screw fixation system are similar to that of PEEK cages with posterior
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BIOMECHANICS instrumentation. ABIF cages also have the inherent properties of osteoconduction and osteoinduction. Therefore, ABIF cages have the appropriate mechanical strength compared with current interbody cages and theoretically retain adequate biological activity.
➢ Key Points Traditional synthetic interbody spacers or corticocancellous ICBG using in PLIF has demonstrated drawbacks including subsidence of metallic cages and donor site morbidity. A novel ABIF cage is prefabricated by morselized small corticocancellous chips. The ABIF cage without supplemental fixation was able to decrease ROM and NZ to near intact levels as well as the ICBG, PEEK cage. When stabilized with pedicle screws, the ABIF cage is biomechanically as stable as ICBG cage and PEEK cage with posterior instrumentation. Although the failure load of PEEK cage was the highest in the axial compression testing, there is no significant difference between the ICBG cage and the ABIF cage.
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