The Effect of Single-Level Disc Degeneration on Dynamic Response of the Whole Lumbar Spine to Vertical Vibration

The Effect of Single-Level Disc Degeneration on Dynamic Response of the Whole Lumbar Spine to Vertical Vibration

Original Article The Effect of Single-Level Disc Degeneration on Dynamic Response of the Whole Lumbar Spine to Vertical Vibration Li-Xin Guo and Wei ...

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Original Article

The Effect of Single-Level Disc Degeneration on Dynamic Response of the Whole Lumbar Spine to Vertical Vibration Li-Xin Guo and Wei Fan

OBJECTIVE: The objective of this study was to investigate the effect of single-level disc degeneration on dynamic response of the whole lumbar spine to vertical whole body vibration that is typically present when driving vehicles.

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METHODS: Ligamentous finite element models of the lumbar L1-S1 motion segment in different grades of degeneration (healthy, mild, and moderate) at the L4-L5 level were developed with consideration of changing disc height and material properties of the nucleus pulpous. All models were loaded with a compressive follower preload of 400 N and a sinusoidal vertical vibration load of 40 N. After transient dynamic analyses, computational results for the 3 models in terms of disc bulge, von-Mises stress in annulus ground substance, and nucleus pressure were plotted as a function of time and compared.

level, and increasing the degeneration did not deteriorate the effect of vertical vibration on the spine.

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RESULTS: All the predicted results showed a cyclic response with time. At the degenerated L4-L5 disc level, as degeneration progressed, maximum value of the predicted response showed a decrease in disc bulge and von-Mises stress in annulus ground substance but a slight increase in nucleus pressure, and their vibration amplitudes were all decreased. At the adjacent levels of the degenerated disc, there was a slight decrease in maximum value and vibration amplitude of these predicted responses with the degeneration.

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CONCLUSIONS: The results indicated that single-level disc degeneration can alter vibration characteristics of the whole lumbar spine especially for the degenerated disc

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Key words Disc degeneration - Dynamic response - Finite element - Follower preload - Lumbar spine - Whole body vibration -

Abbreviations and Acronyms FE: Finite element ROM: Range of motion

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INTRODUCTION

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any cases of low back pain leading to work disability and reduced quality of life are attributed to disc degeneration,1,2 which is related to aging, inadequate nutrition, genetic inheritance, and loading history.3,4 In addition, neurologic degeneration, such as of the sinuvertebral nerve and basivertebral nerve, also affects disc degeneration. An early signal for disc degeneration is a reduction in water and proteoglycan content of the nucleus pulposus, which can decrease the swelling pressure and disc height.5-7 With the progress of degeneration, increased collagen in the nucleus makes it more fibrotic and the nucleus tissue undergoes a process of stiffening.8 The border between the nucleus and annulus gradually becomes diffuse.9 In the degenerated disc, reduced intradiscal pressure caused by the loss of hydration also results in an abnormal stress distribution and large local stress peak in the annulus fibrosus.10,11 These progressive changes of biochemistry and mechanics in the disc inevitably affect biomechanical behavior of the spine. Numerous experimental and numeric studies have been conducted to investigate the biomechanical alterations of lumbar spine with disc degeneration. Experimental studies have shown that disc degeneration could affect multidirectional flexibilities of the lumbar spine. For example, an in vitro study by Kettler et al.12 reported that range of motion (ROM) for the degenerated segment was decreased under flexion-extension and lateral bending but increased under axial

School of Mechanical Engineering and Automation, Northeastern University, Shenyang, China To whom correspondence should be addressed: Li-Xin Guo, Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2017) 105:510-518. http://dx.doi.org/10.1016/j.wneu.2017.06.008 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.

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EFFECT OF SINGLE-LEVEL DISC DEGENERATION

rotation in the early stage of lumbar disc degeneration. With increasing degeneration, the neutral zone ratio (i.e., neutral zone divided by ROM) showed an increase in all 3 loading directions, indicating greater joint laxity.13 An in vivo study by Lee et al.14 examined the effect of single-level and double-level disc degenerations on total lumbar ROM for flexion and extension postures. These investigators found that both degenerations resulted in a significant decrease in total ROM, and the upper lumbar had a larger ROM than the lower lumbar. Finite element (FE) analysis is often used to quantify the effect of disc degeneration on stress and strain responses in the spinal components under physiologic loading conditions.15-19 For example, Kim et al.15 found that with degeneration, disc bulge and maximum strain in annulus fibers for axial compressive loading decreased at the degenerated disc but increased at the adjacent disc. Rohlmann et al.16 showed that for the degenerated disc, increasing the disc degeneration increased maximum von-Mises stress in annulus ground substance for flexion, extension, lateral bending, and axial rotation. Ruberte et al.17 investigated the effect of single-level disc degeneration on its adjacent segments and found that with progressive degeneration, maximum von-Mises and shear stresses at the levels above and below the degenerated one increased for flexion, extension, lateral bending, and axial rotation. However, these previous FE studies mainly focused on determining the effect of disc degeneration on spine biomechanical responses to static loading. Very few have dealt with the condition of whole body vibration, which is typically present when driving vehicles.20-22 Therefore, this study aimed to provide a quantitative investigation of the effect of single-level disc degeneration on dynamic response of the whole lumbar spine to vertical vibration using a developed and validated three-dimensional ligamentous FE model of the lumbar L1-S1 motion segment, allowing simulation of the different grades of degeneration.

METHODS FE Modeling A healthy FE model of the L1-S1 motion segment (Figure 1) was constructed based on computed tomography scans (0.6 mm thick) of a female volunteer without bone diseases and spinal abnormalities. The vertebral body consists of cancellous bone and cortical shell (including end plate) measuring 0.7 mm.23 The intervertebral disc consists of the nucleus pulposus and annulus ground substance comprising 6 fiber layers with a crosswise pattern at 30 from the horizontal.24 The fluidlike behavior of both the nucleus and the annulus ground substance was simulated with the Mooney-Rivlin hyperelastic material law. The contact between the facet joints was approximated by frictionless surface-to-surface contact. The major spinal ligaments and the annulus fibers were modeled as tension-only truss elements. FE models of the lumbar spine representing different grades of disc degeneration (mild and moderate) were generated by decreasing disc height and changing the material property of the nucleus at the L4-L5 level of the healthy model. Based on the disc degeneration grading system of Wilke et al.,25 disc height was assumed to be decreased by 16.5% and 33%, respectively, for mild and moderate degeneration. The reduction in disc height caused a buckle in the fibers and in all the ligaments other than interspinous and supraspinous ligaments that were prestressed. Similar to an FE study by Rohlmann et al.,16 these changes were simulated by offsetting their stress-strain curves. With degeneration, material values of the nucleus approaches that of the annulus ground substance, and the values for mild and moderate degeneration were taken from a study by Schmidt et al.18 Material properties used in the developed FE models were obtained from the published studies18,26-29 and are summarized in Table 1. Validation of the present models was conducted by comparing their predictions with corresponding experimental results in the literature.13,30,31

Figure 1. A finite element model of the whole lumbar spine L1-S1.

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Table 1. Material Properties Used in the Finite Element Models Materials

Young Modulus (MPa)

Poisson Ratio

Density (kg/mm3)

Cross-Sectional Area (mm2)

Element Type

Vertebra Cortical bone

12000

0.3

1.7e-6



S3

Cancellous bone

100

0.2

1.1e-6



C3D4

Posterior bone elements

3500

0.25

1.4e-6



C3D4

Bony end plate

23.8

0.4

1.2e-6



S3

C10 ¼ 0.18, C01 ¼ 0.045



1.05e-6



C3D8

C10 ¼ 0.12, C01 ¼ 0.03 (healthy) C10 ¼ 0.14, C01 ¼ 0.035 (mild) C10 ¼ 0.17, C01 ¼ 0.041 (moderate)



1.02e-6



C3D8

Intervertebral disc Annulus ground substance (Mooney-Rivlin law) Nucleus pulpous (Mooney-Rivlin law) Annulus fiber layers

T3D2

Outermost

550

0.3

1.0e-6

0.7

Second

495

0.3

1.0e-6

0.63

Third

440

0.3

1.0e-6

0.55

Fourth

420

0.3

1.0e-6

0.49

Fifth

385

0.3

1.0e-6

0.41

Innermost

360

0.3

1.0e-6

0.30

Ligaments

T3D2

Anterior longitudinal

7.8 (<12.0%), 20 (>12.0%)



1.0e-6

63.7

Posterior longitudinal

10.0 (<11.0%), 20 (>11.0%)



1.0e-6

20

Ligamentum flavum

15.0 (<6.2%), 19.5 (>6.2%)



1.0e-6

40

Supraspinous

8.0 (<20.0%), 15 (>20.0%)



1.0e-6

30

Interspinous

10.0 (<14.0%), 11.6 (>14.0%)



1.0e-6

40

Intertransverse

10.0 (<18.0%), 58.7 (>18.0%)



1.0e-6

Capsular

7.5 (<25.0%), 32.9 (>25.0%)



1.0e-6

1.8 30

S3, 3-node triangular element; C3D4, 4-node tetrahedral element; C3D8, 8-node hexahedral element; T3D2, 2-node truss element.

Boundary and Loading Conditions The caudal part of the S1 segment in the FE models was fully constrained, and all models were subjected to a compressive follower preload and a sinusoidal vertical load. The compressive follower preload was 400 N and represented the physiologic compressive loading produced by the muscle activities. This preload was applied by decreasing the temperature in thermo-isotropic truss elements placed bilaterally of each motion segment along a path approximating the tangent to curvature of the spine,30,32 as shown in Figure 1. The sinusoidal vertical load of 40 N at a frequency of 5 Hz was applied on the superior surface of the L1 vertebra to simulate the vibration load of the human body based on a study by Wilder et al.33 An equivalent damping ratio of 0.08 was adopted in the models. In addition, to include the effect of upper body mass, a mass point of 40 kg was imposed on the top of the lumbar spine, as suggested by Goel et al.,26 and the point was located on the superior surface of the L1 vertebra 10 mm anterior to the L3-L4 vertebral centroid.34 ABAQUS

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software, version 6.10 (Dassault Systèmes Simulia Corp., Providence, Rhode Island, USA), was used to perform all FE analyses in this study.

RESULTS Validation of the FE Models The healthy FE model was validated by comparing its predictions with the published experimental results under static and cyclic loading conditions. The predicted disc compression under follower load and ROM under bending moments for each motion segment compared well with the experimental data, and most of the predicted results fell within 1 standard deviation of the in vitro values (Figure 2A). Then, the L1-L2, L2-L3, L3-L4 and L4-L5 motion segments were separated from the whole lumbar model and used to perform the cyclic loading validation, respectively.

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Figure 2. Validation of the health finite element model against (A) in vitro experimental data of Renner et al.30 under static loading conditions including follower load of 1200 N, flexion/extension moment of þ8/6 Nm with 800 N follower preload, left-right lateral bending

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moment of 6 Nm and left-right torsion moment of 4 Nm and (B) in vitro experimental data of Stokes and Gardner-Morse31 under sinusoidal anterior-posterior displacement load of 0.6 mm with 642  132 N axial compressive preload.

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These predicted results also showed close agreement with the experimental results (Figure 2B). For the models with a degenerated L4-L5 disc, ROM of the L4L5 level under a bending moment in flexion-extension, lateral bending, and torsion directions was chosen as a parameter for validation. As shown in Figure 3, for both the mild and moderate degeneration, all the predicted ROM except torsion ROM fell within 1 standard deviation of the in vitro values. In addition, as degeneration progressed from mild to moderate, the predicted flexion-extension and lateral bending ROMs were decreased from 10.3 to 9.7 and from 13.2 to 12.1 , respectively, but the predicted torsion ROM was increased from 6.1 to 6.3 .

stress in annulus ground substance, and nucleus pressure at all 5 lumbar disc levels were collected and plotted as a function of time. As shown in Figures 4 and 5, the plots of the predicted results showed a cyclic response with time. The maximum and

Dynamic Response of the Lumbar Spine for Different Grades of Degeneration After transient dynamic analyses, computational results for different grades of degeneration in terms of disc bulge, von-Mises

Figure 3. Comparison of the range of motion (ROM) for the degenerated L4-L5 disc level between the present study and in vitro experiment of Mimura et al.13 under bending moments of 10 Nm.

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Figure 4. The predicted dynamic response at the degenerated L4-L5 disc level under the sinusoidal vertical vibration load for different grades of degeneration.

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Figure 5. The predicted dynamic response at the adjacent levels of the degenerated disc under the sinusoidal

minimum values and vibration amplitudes of these predicted dynamic responses are listed in Table 2. Figure 4 shows that at the degenerated L4-L5 disc level, disc degeneration caused an apparent change in the predicted dynamic responses. Maximum values of the disc bulge and the von-Mises stress in annulus ground substance decreased from 1.084 mm and 0.220 MPa (healthy) to 0.919 mm and 0.196 MPa (mild), and 0.633 mm and 0.175 MPa (moderate), respectively, with increasing degeneration. Maximum value of the nucleus increased from 0.576 MPa (healthy) to 0.587 MPa (mild) and 0.611 MPa (moderate) with the degeneration. Vibration amplitudes of all the predicted responses at the degenerated disc decreased as degeneration progressed, and the decreasing effect of moderate degeneration reached 48.8% in the disc bulge, 28.9% in the von-Mises stress in annulus ground substance, and 11.4% in nucleus pressure. At the adjacent levels of the degenerated disc, variations of the predicted dynamic response caused by the degeneration, by

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vertical vibration load for different grades of degeneration.

contrast, were slight, as shown in Figure 5. A small decrease in maximum values and vibration amplitudes of the L1-L2, L2-L3, L3-L4, and L5-S1 levels was observed as degeneration progressed. For example, at level L5-S1, moderate degeneration decreased maximum values of the disc bulge, von-Mises stress in annulus ground substance, and nucleus pressure by 1.7%, 0.78%, and 0.91%, respectively. The corresponding decrease in their vibration amplitudes was 10.9%, 2.2%, and 2.7%, respectively. DISCUSSION Three-dimensional ligamentous FE models of the whole lumbar spine L1-S1 in different grades of single-level disc degeneration (healthy, mild, and moderate) were initially developed by changing geometry and associated material properties of the L4-L5 motion segment. Subsequently, these models were used to study the effect of disc degeneration on the time-domain

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Table 2. Maximum and Minimum Values and Vibration Amplitudes of the Predicted Dynamic Response During the Sinusoidal Vertical Vibration Load for Different Grades of Degeneration Maximum Response Disc bulge (mm)

Von-Mises stress in annulus ground substance (MPa)

Nucleus pressure (MPa)

Minimum

Vibration Amplitude*

Disc Level

Healthy

Mild

Moderate

Healthy

Mild

Moderate

Healthy

Mild

Moderate

L1-L2

0.889

0.885

0.878

0.544

0.564

0.569

0.345

0.321

0.309

L2-L3

0.740

0.735

0.729

0.432

0.449

0.457

0.308

0.286

0.272

L3-L4

0.680

0.675

0.669

0.382

0.394

0.402

0.298

0.281

0.267

L4-L5

1.084

0.919

0.633

0.697

0.641

0.435

0.387

0.278

0.198

L5-S1

1.154

1.142

1.134

0.722

0.749

0.749

0.432

0.393

0.385

L1-L2

0.220

0.218

0.216

0.124

0.130

0.132

0.096

0.088

0.084

L2-L3

0.211

0.210

0.208

0.120

0.128

0.130

0.091

0.082

0.078

L3-L4

0.191

0.190

0.188

0.110

0.118

0.119

0.081

0.072

0.069

L4-L5

0.220

0.196

0.175

0.130

0.125

0.111

0.090

0.071

0.064

L5-S1

0.257

0.257

0.255

0.167

0.167

0.167

0.090

0.090

0.088

L1-L2

0.721

0.715

0.707

0.371

0.395

0.403

0.350

0.320

0.304

L2-L3

0.668

0.662

0.655

0.341

0.368

0.376

0.327

0.294

0.279

L3-L4

0.586

0.581

0.575

0.307

0.333

0.339

0.279

0.248

0.236

L4-L5

0.576

0.587

0.611

0.303

0.345

0.369

0.273

0.242

0.242

L5-S1

0.661

0.661

0.655

0.364

0.364

0.366

0.297

0.297

0.289

*Vibration amplitude ¼ maximumminimum.

dynamic response of the whole lumbar spine to a sinusoidal vertical vibration load, which has rarely been analyzed in the existing literature. To simulate physiologic compressive loading on the whole lumbar spine without generating instability, the follower load technique30,32 was used and all the developed models were subjected to a compressive follower preload. The healthy and degenerated FE models were validated against the published experimental results under the same loading conditions. Figures 2 and 3 show that most of the model predictions compared well with the in vitro values. Some discrepancies between the FE and experimental results may be because the intervertebral discs at different levels of the lumbar cadaver specimen often have different grades of degeneration, and this was not considered in the models. Moreover, the discs become dry and stiff during in vitro tests because of their viscoelastic nature, which was also not considered and might lead to the observed discrepancies. Figure 3 also shows that ROM of the degenerated disc showed a decrease in flexion-extension and lateral bending but a slight increase in torsion with increasing the disc degeneration. These results were consistent with the findings of previous in vitro studies.12,13 In modern times, an increasing part of the population is exposed to whole body vibration in vehicles. Investigations have shown that the vibration load may markedly increase the stress and strain within the discs compared with the static load with equivalent magnitude26,35 and might thus trigger the bone remolding process and result in spinal disorders.20 Therefore,

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the vibration load was often considered to be more dangerous for the human spine than static load. In this study, a comparison of time-domain dynamic response to vertical vibration between the healthy and degenerated spine models was conducted. Degeneration affected the predicted response of both the degenerated disc and the adjacent disc levels (Figures 4 and 5). At the degenerated L4-L5 level, the present results suggested that with increasing degeneration, from healthy to moderate, maximum values of the disc bulge and the von-Mises stress in annulus ground substance decreased by 41.6% and 20. 5%, respectively. Kim et al.15 predicted the same trends for disc bulge and annulus stress of the degenerated disc under an axial compressive load. In addition, maximum values of the nucleus pressure at the degenerated disc increased by a small percentage (6.1%) as a result of moderate degeneration. Lu et al.27 and Natarajan and Andersson36 reported a similar conclusion: for a disc with lower height, the nucleus pressure was slightly higher under compression loading. At the adjacent levels of the degenerated disc, the predicted response showed minimal variations with increasing degeneration, and a slight decrease was observed in their maximum values. Similar finding have also been shown by Kumaresan et al.37 using an FE model of the C4-C6 cervical spine under compression. Table 2 shows that at all 5 spinal levels, vibration amplitudes of all the predicted response decreased with degeneration. This finding implies that single-level disc degeneration does not deteriorate the effect of vertical vibration on the spine.

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ORIGINAL ARTICLE LI-XIN GUO AND WEI FAN

EFFECT OF SINGLE-LEVEL DISC DEGENERATION

There were some limitations in this study. First, the degenerative changes caused by osteophytes, sclerosis, and annular tears were neglected in the degenerated FE models.5 Second, muscles were not included in the model. Although using the follower load technique may mitigate this limitation, it could not entirely replace complex contributions of the muscles to spinal responses. In addition, because of lack of a data source for the time-domain dynamic response of the lumbar motion segment under sinusoidal vertical loading, validation of the present model was performed only under sinusoidal anterior-posterior loading.

response of the whole lumbar spine to vertical vibration using a developed and validated L1-S1 FE model with different grades of degeneration at the L4-L5 disc. The results suggest that degeneration altered the predicted dynamic responses and their vibration amplitudes at both the degenerated disc and the adjacent disc levels, whereas it did not deteriorate the effect of vertical vibration on these levels. The findings may be useful in understanding vibration characteristics of the lumbar spine with degenerated disc.

CONCLUSIONS

ACKNOWLEDGMENTS

The present study quantitatively investigated the effect of single-level disc degeneration on time-domain dynamic

We are grateful for the grants from the National Natural Science Foundation of China (51275082, 11272273).

REFERENCES 1. Luoma K, Riihimaki H, Luukkonen R, Raininko R, ViikariJuntura E, Lamminen A. Low back pain in relation to lumbar disc degeneration. Spine (Phila Pa 1976). 2000;25:487-492. 2. Freemont AJ. The cellular pathobiology of the degenerate intervertebral disc and discogenic back pain. Rheumatology. 2009;48:5-10. 3. Adams MA, Roughley PJ. What is intervertebral disc degeneration, and what causes it? Spine (Phila Pa 1976). 2006;31:2151-2161.

replacement with varying degrees of nucleotomy. J Biomech Eng. 2014;36:051001.

back pain (1986e1997). Int Arch Occup Environ Health. 1999;72:351-365.

12. Kettler A, Rohlmann F, Ring C, Mack C, Wilke HJ. Do early stages of lumbar intervertebral disc degeneration really cause instability? Evaluation of an in vitro database. Eur Spine J. 2011;20:578-584.

21. Magnusson ML, Pope MH, Wilder DG, Areskoug B. Are occupational drivers at an increased risk for developing musculoskeletal disorders? Spine (Phila Pa 1976). 1996;21:710-717.

13. Mimura M, Panjabi MM, Oxland TR, Crisco JJ, Yamamoto I, Vasavada A. Disc degeneration affects the multidirectional flexibility of the lumbar spine. Spine (Phila Pa 1976). 1994;19: 1371-1380.

4. Kalb S, Martirosyan NL, Kalani MYS, Broc GG, Theodore N. Genetics of the degenerated intervertebral disc. World Neurosurg. 2012;77: 491-501.

14. Lee SH, Daffner SD, Wang JC. Does lumbar disk degeneration increase segmental mobility in vivo? Segmental motion analysis of the whole lumbar spine using kinetic MRI. J Spinal Disord Tech. 2014; 27:111-116.

5. Benneker LM, Heini PF, Anderson SE, Alini M, Ito K. Correlation of radiographic and MRI parameters to morphological and biochemical assessment of intervertebral disc degeneration. Eur Spine J. 2005;14:27-35.

15. Kim YE, Goel VK, Weinstein JN, Lim TH. Effect of disc degeneration at one level on the adjacent level in axial mode. Spine (Phila Pa 1976). 1991;16: 331-335.

6. Frobin W, Brinckmann P, Kramer M, Hartwig E. Height of lumbar discs measured from radiographs compared with degeneration and height classified from MR images. Eur Radiol. 2001;11: 263-269.

16. Rohlmann A, Zander T, Hendrik Schmidt H, Wilke HJ, Bergmann G. Analysis of the influence of disc degeneration on the mechanical behaviour of a lumbar motion segment using the finite element method. J Biomech. 2006;39: 2484-2490.

7. Urban JP, McMullin JF. Swelling pressure of the lumbar intervertebral discs: influence of age, spinal level, composition, and degeneration. Spine (Phila Pa 1976). 1988;13:179-187. 8. Inoue N, Espinoza Orias AA. Biomechanics of intervertebral disk degeneration. Orthop Clin North Am. 2011;42:487-499.

17. Ruberte LM, Natarajan RN, Andersson GB. Influence of single-level lumbar degenerative disc disease on the behavior of the adjacent segmentsa finite element model study. J Biomech. 2009;42: 341-348.

9. Adams MA, Bogduk N, Burton K, Dolan P. The biomechanics of back Pain. Philadelphia, PA: Churchill Livingstone; 2002.

18. Schmidt H, Kettler A, Rohlmann A, Claes L, Wilke HJ. The risk of disc prolapses with complex loading in different degrees of disc degeneration-a finite element analysis. Clin Biomech. 2007;22: 988-998.

10. Adams MA, McNally D, Dolan P. Stress distributions inside intervertebral discs the effect of age and degeneration. J Bone Joint Surg. 1996;78: 965-972.

19. Wang L, Zhang BK, Chen S, Lu XH, Li ZY, Guo QF. A validated finite element analysis of facet joint stress in degenerative lumbar scoliosis. World Neurosurg. 2016;95:126-133.

11. Cannella M, Isaacs JL, Allen S, Orana A, Vresilovic E, Marcolongo M. Nucleus implantation: the biomechanics of augmentation versus

20. Bovenzi M, Hulshof CT. An updated review of epidemiologic studies on the relationship between exposure to wholebody vibration and low

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22. Lis AM, Black KM, Korn H, Nordin M. Association between sitting and occupational LBP. Eur Spine J. 2007;16:283-298. 23. El-Rich M, Arnoux PJ, Wagnac E, Brunet C, Aubin CE. Finite element investigation of the loading rate effect on the spinal load-sharing changes under impact conditions. J Biomech. 2009;42:1252-1262. 24. Goel VK, Monroe T, Gilbertson LG, Brinckmann P, Nat R. Interlaminar shear stresses and laminae separation in a disc. Finite-element analysis of the L3-L4 motion segment subjected to axial compressive loads. Spine (Phila Pa 1976). 1995;20:689-698. 25. Wilke HJ, Rohlmann F, Neidlinger-Wilke C, Werner K, Claes L, Kettler A. Validity and interobserver agreement of a new radiographic grading system for intervertebral disc degeneration: Part I. Lumbar spine. Eur Spine J. 2006;15: 720-730. 26. Goel VK, Park H, Kong WZ. Investigation of vibration characteristics of the ligamentous lumbar spine using the finite element approach. J Biomech Eng. 1994;116:377-383. 27. Lu YM, Hutton WC, Gharpuray VM. Can variations in intervertebral disc height affect the mechanical function of the disc? Spine (Phila Pa 1976). 1996;21:2208-2216. 28. Polikeit A, Ferguson SJ, Nolte LP, Orr TE. Factors influencing stresses in the lumbar spine after the insertion of intervertebral cages: finite element analysis. Eur Spine J. 2003;12: 413-420. 29. Wu YG, Wang YH, Wu JH, Guan JJ, Mao NF, Lu CW, et al. Study of double-level degeneration of lower lumbar spines by finite element model. World Neurosurg. 2016;86:294-299.

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30. Renner SM, Natarajan RN, Patwardhan AG, Havey RM, Voronov LI, Guo BY, et al. Novel model to analyze the effect of a large compressive follower pre-load on range of motions in a lumbar spine. J Biomech. 2007;40:1326-1332.

31. Stokes IAF, Gardner-Morse M. A database of lumbar spinal mechanical behavior for validation of spinal analytical model. J Biomech. 2016;49: 780-785.

32. Patwardhan AG, Havey R, Dunlap B. A follower load carrying capacity of the compression. Spine (Phila 1003-1009.

518

Meade KP, Lee B, increases the loadlumbar spine in Pa 1976). 1999;24:

www.SCIENCEDIRECT.com

33. Wilder DG, Woodworth BB, Frymoyer JW, Pope MH. Vibration and the human spine. Spine (Phila Pa 1976). 1982;7:243-254. 34. Shirazi-Adl A, Parnianpour M. Role of posture in mechanics of the lumbar spine in compression. J Spinal Disord. 1996;9:277-286. 35. Guo LX, Teo EC, Lee KK, Zhang QH. Vibration characteristics of the human spine under axial cyclic loads: effect of frequency and damping. Spine (Phila Pa 1976). 2005;30: 631-637. 36. Natarajan RN, Andersson GB. The influence of lumbar disc height and cross-sectional area on the mechanical response of the disc to physiologic loading. Spine (Phila Pa 1976). 1999;24: 1873-1881.

37. Kumaresan S, Yoganandan N, Pintar FA, Maiman DJ, Goel VK. Contribution of disc degeneration to osteophyte formation in the cervical spine: a biomechanical investigation. J Orthop Res. 2001;19:977-984. Conflict of interest statement: Funding was received from the National Natural Science Foundation of China (51275082, 11272273). Received 21 March 2017; accepted 1 June 2017 Citation: World Neurosurg. (2017) 105:510-518. http://dx.doi.org/10.1016/j.wneu.2017.06.008 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2017 Elsevier Inc. All rights reserved.

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