The biomechanical influence of anterior vertebral body osteophytes on the lumbar spine: A finite element study

Accepted Manuscript

The biomechanical influence of anterior vertebral body osteophytes on the lumbar spine: a finite element study Kuan Wang , Chenghua Jiang , Lejun Wang , Huihao Wang , Wenxin Niu PII: DOI: Reference:

S1529-9430(18)30646-6 10.1016/j.spinee.2018.07.001 SPINEE 57747

To appear in:

The Spine Journal

Received date: Revised date: Accepted date:

20 February 2018 2 July 2018 2 July 2018

Please cite this article as: Kuan Wang , Chenghua Jiang , Lejun Wang , Huihao Wang , Wenxin Niu , The biomechanical influence of anterior vertebral body osteophytes on the lumbar spine: a finite element study , The Spine Journal (2018), doi: 10.1016/j.spinee.2018.07.001

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

The biomechanical influence of anterior vertebral body osteophytes on the lumbar spine: a finite element study

CR IP T

Authors: Kuan Wang a, b, Chenghua Jiang b, Lejun Wang c, Huihao Wang d, Wenxin Niu b

a Yangzhi Rehabilitation Hospital, Sunshine Rehabilitation Centre, Tongji University School of Medicine, Shanghai 201619, China; b Biomechanics Laboratory, Tongji University School of Medicine, Shanghai 200092, China;

AN US

c Sport and Health Research Center, Physical Education Department, Tongji University, Shanghai 200092, China; d Shi’s Center of Orthopedics and Traumatology, Shuguang Hospital Affiliated to Shanghai University of TCM, Shanghai 201203, China;

M

Corresponding authors:

ED

Wenxin Niu, PhD, Associate professor,

Biomechanics Laboratory, Tongji University School of Medicine, Shanghai 200092, China.

PT

Tel.: (86)021-65982856

CE

E-mail address: [email protected]

AC

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 11672211), and the Fundamental Research Funds for the Central Universities (No. 1500219130) with no relevant conflicts of interest.

Abstract 1 / 26

ACCEPTED MANUSCRIPT

Background Context: Anterior vertebral body osteophytes are common with degeneration but their biomechanical influence on the whole lumbar spine remains

CR IP T

unclear.

Purpose: To investigate the biomechanical influence of anterior vertebral body

AN US

osteophytes on the whole lumbar spine.

Study Design/Setting: This is a study using finite element analysis.

M

Outcome Measures: Intersegmental rotation, maximum Mises stress and intradiscal

ED

pressure on the intervertebral discs of different lumbar levels were calculated.

PT

Methods: A finite element model of an intact lumbar spine was constructed and validated against in vitro studies. The modified models, which had different degrees

CE

of anterior vertebral body osteophyte formation in combination with disc space

AC

narrowing, were applied with physiological loadings.

Results: The lumbar levels with various degrees of osteophyte formation altered the kinematics of these levels, which also affected the whole lumbar spine. In flexion and lateral bending, the segment that was one level inferior to the vertebra with osteophyte formation showed a trend towards increased range of motion. On the intervertebral 2 / 26

ACCEPTED MANUSCRIPT

discs that were one level inferior to the osteophyte formation level, a trend towards increase in the maximum von Mises stress was found on the annulus.

Conclusions: Segments adjacent to levels with anterior vertebral body osteophytes

CR IP T

showed increased intersegmental rotation and maximum stress. Further clinical observation should be performed to verify the results in vivo.

AN US

Keywords: Osteophyte; Degeneration; Lumbar spine; Intervertebral disc; Finite element analysis.

AC

CE

PT

ED

M

Classifications: Basic Science

3 / 26

ACCEPTED MANUSCRIPT

Introduction Osteophytes, also called bone spurs, are often observed in clinically and radiologically. Spinal osteophytes have been reported in up to 80% of men and 60%

CR IP T

of women aged 50 years [1]. In the lumbar region, the prevalence of vertebral body osteophytes was found to increase with aging [2, 3]. Vertebral body osteophytes are considered to be secondary to the degenerative process of the spine [4]. Osteophyte

AN US

formation has been found to be associated with other features of disc degeneration, such as disc space narrowing [5]. Vertebral body osteophytes most often occur on the anterior edge of vertebral body (30.4% on the superior and 25.2% on the inferior

M

surface), while osteophytes on the posterior side are less prevalent [2]. Clinicians may consider the presence of osteophytes in two different ways. One

ED

is to view them as a sign of spinal instability [6]. Macnab et al. [7] found that small

PT

developing osteophytes were associated with spinal instability. Experiments in animals have shown that scalpel-induced disc degeneration leads to osteophytes

CE

growing into adjacent vertebrae [8]. Others have considered osteophytes as the body’s

AC

way of reducing intersegmental movements of a spinal level [9]. Al-Rawahi et al. [10] examined the stiffness of motion of segments from T5-T6 to L3-L4 and found a significant decrease in stiffness following the removal of osteophytes. Similar findings were also demonstrated by finite element (FE) analysis, in which the range of motion (ROM) was decreased in a severely degenerated L4-L5 FE model with osteophytes [11]. 4 / 26

ACCEPTED MANUSCRIPT

Although vertebral body osteophytes may be an adaptive remodeling process that reduces stress on a degenerated intervertebral disc that leads to a change in stiffness of the affected lumbar level, its mechanical influence on the whole lumbar spine remains unclear. It is known that some lumbar interventions, such as vertebroplasty or

CR IP T

interbody fusion also result in a change in flexibility of that lumbar level. Biomechanical analyses have found that they not only affect the biomechanics of the osteophytic level but the adjacent level as well [12-14]. Therefore, one could

AN US

speculate that vertebral body osteophytes may affect adjacent levels in a similar way. The objective of this study was to evaluate the biomechanical response of the lumbar spine with different degrees of anterior vertebral body osteophyte formation at

M

each level. A subject-specific male lumbar FE model was constructed and validated. The modified FE models with anterior vertebral body osteophytes were first validated

ED

and then subjected to different physiological loads so that changes in intersegmental

PT

rotation (ISR) and intervertebral disc stress/pressure could be evaluated. It was hypothesized that osteophyte formation would influence the segmental kinematics and

AC

CE

stress/pressure on the disc of the adjacent levels.

Materials and methods FE modeling Computed tomography slices which were imaged at 0.625 mm intervals from L1 to the sacrum of a 29-year old male subject in a supine position were extracted from the institutional medical imaging system for model construction. This subject did not 5 / 26

ACCEPTED MANUSCRIPT

have fracture, spondylolisthesis or other anatomical disorders. Mean lordosis from L1-L5 was 25.5°, which was comparable with previously reported FE models (ranging from 19.1° to 44.0°) [15]. Ethical approval was attained for scientific use of the data from the Institutional Ethics Board of Tongji University School of Medicine.

CR IP T

The images were first imported into Mimics 10.1 software (Materialise Inc., Leuven, Belgium) to create binary STL files, which were then imported into Geomagic Studio 11 (Geomagic, Inc., Research Triangle Park, NC, USA) for further

AN US

smoothing and creation of surface models. Finite element meshing was performed using Hypermesh 11.0 (Altair Engineering, Inc., Executive Park, CA, USA). The intervertebral discs and ligaments were then created according to the anatomy of the

M

lumbar spine [16].

The vertebrae, consisting of endplate cartilage and cortical and cancellous bone,

ED

were modeled with isotropic, linear mechanical properties. The thickness of the

PT

cortical bone was approximately 0.5 mm [17]. The cartilaginous endplates were modeled to be approximately 0.6 mm thick [18]. Frictionless surface-to-surface

CE

contacts were created between the articular facets. The initial gap between the facet

AC

joints was approximately 0.5 mm [15]. Intervertebral discs are composed of an incompressible nucleus pulposus, an

annulus ground substance and embedded fibers. The center of the nucleus was offset dorsally from the midpoint in the mid sagittal plane of the disc by around 3.5 mm [19]. The nucleus pulposus was modeled as a fluid cavity which constituted approximately 44% of the disc volume with a bulk modulus of 2000 MPa [20]. The annulus fibers 6 / 26

ACCEPTED MANUSCRIPT

were modeled as rebar elements and the volume content of fibers with respect to the surrounding ground substance was assumed to vary from 23% at the outer layer to 5% at the inner fiber layer. The fibers in different annulus layers were weighted (outermost layers 1–2: 1.0, layers 3–4: 0.9, layers 5–6: 0.75, innermost layers 7–8:

CR IP T

0.65) [19]. The orientation of fibers was ±35° with respect to the transversal plane of each disc [21]. The annulus ground substance was modeled with nonlinear hyperelastic mechanical properties (C1=0.18, C2=0.045) [19]. All ligaments were

AN US

modeled as nonlinear connector elements.

A convergence test indicated that the finite element solution was accurate using a model with 82,595 nodes and 201,414 elements (Fig. 1). The differences in ISR, von

M

Mises stress and intradiscal pressure (IDP) within 5% was defined as achieving a

Table 1.

PT

Model validation

ED

satisfactory accuracy. Detailed material properties assigned to the model are listed in

To validate the FE model, the predicted ROMs under different loading conditions

CE

were compared against values observed in in vitro studies [25, 26]. All degrees of

AC

freedom of the sacrum were constrained throughout the whole analysis. Pure moments of 7.5 Nm were applied to L1 in the three planes to produce flexion, extension, axial rotation and lateral bending. The intradiscal pressure at L4-L5 was validated by applying a compressive follower load of 1000 N between the L4 and L5 levels [27]. The validation and FE analyses that followed were performed using Abaqus v6.14 (Simulia Inc., Providence, RI, USA). 7 / 26

ACCEPTED MANUSCRIPT

FE analysis Three grades of osteophyte lengths with disc space narrowing were modeled with reference to the grading system of Wilke et al. [28], to represent mild (Grade 1),

CR IP T

moderate (Grade 2) or severe (Grade 3) anterior vertebral body osteophyte formation (Fig. 2). The three grades were modeled coupled with disc height loss of 16.5%, 49.5% and 82.5%, respectively. To adjust the geometrical features of the intervertebral disc,

AN US

the disc height was reduced in the Hypermesh software according to the grading system. The elements representing the substance between the osteophytes were

created at the anterior edge of intervertebral disc and its length in the mid sagittal

M

plane was set corresponding to the disc height loss. Then, the elements representing the anterior vertebral body osteophytes above or below were created accordingly, and

ED

the length of osteophytes was equal to the height decrease of the intervertebral space

PT

[11]. We assumed that the nucleus-annulus volume ratio was not changed within different osteophyte grades.

CE

Because the annular fibers and most ligaments began to buckle when the disc

AC

height decreased [20], the stress-strain curves of the annular fibers and the force-displacement curves of the ligaments were offset (expanding the toe region of the curves) to simulate the buckled fibers and ligaments [11]. Therefore, the fibers and ligaments got stretched after they reached their original length. The compressibility of 0.0005 mm2/N for healthy nucleus pulposus increased to 0.0503 mm2/N, 0.0995 mm2/N, and 0.1500 mm2/N in the mild, moderate and severe anterior vertebral body 8 / 26

ACCEPTED MANUSCRIPT

osteophyte models, respectively [20]. The Young’s modulus of the osteophytes was set to 500 MPa with a Poisson’s ratio of 0.2, while the material properties of the structure between the osteophytes was set at c1=0.19 and c2=0.045 [11]. The ROMs of segments with osteophytes and disc height narrowing were first

CR IP T

validated against the results in the literature by adding 7.5-Nm pure moment in three principle axes [29]. To simulate flexion, extension, axial rotation and lateral bending under upper body weight and muscle contraction, all lumbar FE models (one intact

AN US

and fifteen osteophyte models) were subjected to four physiological loading patterns, each of which included a follower load in combination with bending moment [15]. The detailed loading modes are shown in Table 2. For each model, the ISR of the

M

osteophytic level and other levels in the lumbar spine (three levels superior and inferior to the osteophytic level) were calculated and compared against each other.

ED

Additionally, the IDP and maximum von Mises stress on the nearest three levels of

PT

intervertebral discs under flexion and extension were also calculated. To test the reliability of the results in the adjacent segments, a sensitivity study was performed

CE

with different degrees of L4-L5 osteophytes under the aforementioned physiological

AC

loading modes. The offset of stress-strain curves of annular fibers, force-displacement curves of ligaments and bulk modulus of nucleus pulposus were increased by 25% and decreased by 25%. The ISR under 4 physiological loading modes, IDP and maximum von Mises stress under flexion and extension of the adjacent segments were acquired and the differences to the original osteophyte models were calculated.

9 / 26

ACCEPTED MANUSCRIPT

Results The total ROM and ISR of flexion, extension, axial rotation and lateral bending under 7.5-Nm pure moments were validated against published results (Fig. 3). The total ROMs in three principal axes predicted by the FE computation were within the

CR IP T

ranges reported by Rohlmann et al. [25]. The ISRs at different lumbar levels were most within the ranges of one standard deviation reported by Panjabi et al. [26], and some ISRs (L4-L5 and L5-S1 in extension) were within the ranges of two standard

AN US

deviations. The L1-L2 ISR in flexion and L5-S1 ISR in axial rotation were 7.17° and 1.58° respectively, which were overpredicted compared with in vitro data. L4-L5 IDP increased under 1000 N compressive force which was in agreement with the results of

M

the in vitro study [27].

Under the 7.5-Nm pure moment, the ISRs of segments with grade 3 osteophytes

ED

were within the ranges reported by Volkheimer et al. [29] (Fig. 4). The predicted ISRs

PT

of segments with grade 1 and grade 2 osteophyte formations in flexion-extension and lateral bending were higher than the in vitro data and the mean ISR of segments with

CE

grade 1 osteophytes in axial rotation were within the reported range. Osteophytes

AC

combined with disc space narrowing greatly reduced the flexion and lateral bending ISR of the corresponding lumbar level with severe osteophytes and reduced the flexion ISR of the level with mild and moderate osteophytes (Fig. 5). Under the physiological loading of extension and axial rotation, the ISR of the lumbar levels with different degrees of osteophytes all increased, but the ISR of the level with severe osteophytes increased the least compared with the original FE model. 10 / 26

ACCEPTED MANUSCRIPT

The changes in ISR of the other lumbar levels were pooled according to their positions in relation to osteophyte level (Fig. 6). The segments below the osteophytic levels demonstrated a trend of increased ISR in flexion (0.40-1.28%) and lateral bending (0.36-1.76%), and the segments above the osteophytic levels also showed a

CR IP T

trend of increased ISR in extension (0.41-1.91%). In axial rotation, the mean values were 1.53±3.11% one level above and 0.18±1.00% one level below.

In flexion and extension, although anterior vertebral body osteophytes appeared

AN US

to decrease the IDP of the segments that were one level above or below, a trend could be observed that osteophytes increased the maximum von Mises stress on the annulus ground substance which was one level below it in the moderate and severe osteophyte

M

models (Fig. 7).

In the sensitivity study, the adjustments of the selected material properties in

ED

L4-L5 segment with anterior vertebral body osteophytes caused differences in ISR,

PT

IDP and the maximum von Mises stress changes of adjacent segments (supplemental material Fig. A-C). The maximum differences were less than 0.315% in ISR, 0.082%

CE

in IDP and 0.196% in the maximum von Mises stress compared to that of the original

AC

osteophyte models.

Discussion The current study investigated the biomechanical influence of one segment of anterior vertebral body osteophytes on the whole lumbar spine through an FE analysis. The modified FE models with different degrees of osteophytes in combination with 11 / 26

ACCEPTED MANUSCRIPT

disc space narrowing were applied with physiological loadings. The results showed that the various degrees of osteophytes changed the kinematics of this lumbar level, and also had an effect on the kinematics, maximum Mises stress and IDP of adjacent levels. The sensitivity study showed that the predictions about the changes of the

CR IP T

adjacent segments in the current study were less affected by the adjustment of material properties of annular fibers, nucleus pulposus and ligaments. Therefore, the results related to the adjacent segments were most probably due to the combined

AN US

effect of osteophytes, substance between osteophytes and disc height narrowing. These results give insights into the contribution of lumbar osteophytes to the process of degeneration of the whole lumbar region.

M

Lumbar osteophytes are most common at the anterior edge of the vertebral body [2]. We found that anterior vertebral body osteophytes with disc space narrowing

ED

greatly decreased flexion ROM, especially in severe osteophyte formation. The results

PT

showed that the grade 1 anterior vertebral body osteophyte formation decreased the flexion ROM by 0.3°, and the flexion ROM further decreased in grade 2 and grade 3

CE

osteophyte models (1.15° and 3.99°, respectively). Schmidt et al. [11] reported an

AC

increase of 0.5° in flexion in mildly degenerated disc, and heavy decrease in moderately degenerated disc and severely degenerated disc with osteophytes under 7.5-Nm moment. Volkheimer et al. [29] reported a slight increase in flexion-extension ROM in mildly degenerated disc but heavy decrease was found in moderately and severely degenerated disc. Miura et al. [30] reported that the higher degree of degeneration, the more decrease in flexion-extension ROM under 10-Nm moment. 12 / 26

ACCEPTED MANUSCRIPT

Our results in flexion were generally in agreement with other FE and in vitro studies with similar osteophyte grading systems. Under lateral bending in the current study, the ROMs of the lumbar levels with severe osteophytes had a substantial decrease (2.14°), which was also consistent with the data reported by Schmidt et al. [11] and

CR IP T

Miura et al. [30]. However, in extension, our data showed a trend towards increase in ROM with grade 1 and grade 2 models, while Schmidt et al. [11] and Volkheimer et al. [29] showed an increase in ROM of lumbar segments with grade 1 osteophytes but the

AN US

ROM decreased in segments with grade 2 osteophytes in the sagittal plane. This is

likely related to the difference of osteophyte position between their study and ours. The model of Schmidt et al. [11] and the specimen of Volkheimer et al. [29] included

considered in the current study.

M

osteophytes in other regions, but only anterior vertebral body osteophytes were

ED

These results indicate that anterior vertebral body osteophytes and the structure

PT

between them may serve as a “cushion,” which could resist flexion moment. In grade 3 osteophyte formation with severe disc height narrowing, the ROM further decreased

CE

due to restriction caused by the bony structures. In the current study, mild and

AC

moderate osteophytes were found to increase ROM in axial rotation and extension. This result was similar to those reported by Volkheimer et al. [29]. This was because the decrease in disc height was set to be equal to the length of the osteophytes in the present FE model, and the fibers in the ligaments and annulus were buckled corresponding with the narrowing of the disc space [11]. Although the structure between the osteophytes, which was modeled as annulus ground substance may 13 / 26

ACCEPTED MANUSCRIPT

provide some resistance against axial rotation moment [11], it cannot compensate for the tensile force originally provided by the ligaments and annular fibers. With severe osteophytes, the structure between the osteophytes, along with disc height narrowing, could restrict axial rotation to some extent. This led to a greatly decreased ROM

CR IP T

under axial rotation and extension moment in the grade 3 osteophyte model compared with those of grade 1 and 2.

Lumbar stability is important for the health of the lower back. It includes the

AN US

control subsystem, active subsystem (spinal muscles) and passive subsystem (soft

tissue including ligaments, intervertebral discs, etc.) [31]. Since the loadings applied to each osteophyte model were the same, the ROM under physiological loading

M

reflected the lumbar stiffness provided by the passive subsystem. In the current study, compared with the intact healthy model, the lumbar level with mild and moderate

ED

osteophyte formation and disc space narrowing had a smaller ROM in flexion, but

PT

larger ROM in extension, axial rotation and lateral bending. These results are more supportive of the view that osteophytes, especially mild and moderate ones, are a sign

CE

of instability [7]. However, in the severe model, extension and axial rotation ROMs

AC

largely decreased compared to the mild and moderate models, and it exhibited much less ROM in flexion and lateral bending. Therefore, in cases of severe osteophytes coupled with great disc height narrowing, the motion segment became hypomobile under the loads. Compared with the hypermobility with mild osteophytes, this hypomobility could be viewed as a sign of regaining stability of this spinal segment. Generally, the results of the current study correspond well with the degenerative 14 / 26

ACCEPTED MANUSCRIPT

stages of the spine proposed by Kirkaldy-Willis and Farfan [9], including dysfunction, the unstable phase and stabilization phase. Osteophytes with disc space narrowing were found to influence the kinematics of the adjacent levels as well (Fig. 6). In the current study, the kinematic changes

CR IP T

compared with the original model showed a large variation among different levels. However, in flexion and lateral bending, the segments that were one level inferior to

the osteophytic levels showed a trend of increased ROM. In extension, the segments

AN US

that were one level superior to the osteophytic levels showed a similar trend of

increased ROM. The ROMs further increased in the models with greater osteophyte formation and disc space narrowing. Compared with non-adjacent levels, the increase

M

in ROM was clearer in the adjacent level to the osteophytic segments. In clinics, radiological studies also found that the correlation coefficients were greater between

ED

adjacent vertebrae compared with those that were non-adjacent for osteophytes [5].

PT

Furthermore, this effect on adjacent levels may be more pronounced when there is greater osteophyte formation and disc space narrowing. Thus, severe osteophytes

CE

combined with disc height narrowing could be thought of as two aspects of spinal

AC

stability. It may stabilize the affected lumbar level through decreased ROM, while increasing the ROM of adjacent levels. This dysfunction of lumbar passive system in adjacent levels may lead to instability of the segments in clinical scenarios, when the neural controlling system and lumbar muscles cannot compensate properly. Movements in the sagittal plane (flexion and extension) of the lumbar spine are most commonly experienced during daily activities. In the current study, the IDP of 15 / 26

ACCEPTED MANUSCRIPT

the adjacent levels was found to decrease under physiological flexion and extension moment. However, in intervertebral discs that were one level inferior to the osteophytic level, a trend of increasing maximum Mises stress was observed in the annulus. This result suggests that the physiological load produced by compressive

CR IP T

follower load and moment on these lumbar levels were altered by the levels with osteophyte formation, transferring more load onto the annulus of these levels.

Therefore, combining the results of the current study, the osteophytes of one lumbar

AN US

level may contribute to the degeneration of adjacent levels, through enlarged ROM and maximum Mises stress on the annulus.

Several limitations exist in the current study. First, this was a theoretical

M

computational prediction of the biomechanical effects of anterior vertebral body osteophytes with disc space narrowing on the lumbar spine. Observational studies of

ED

the clinical changes with lumbar degeneration should be performed to further verify

PT

these results. Second, we simulated different degrees of anterior vertebral body osteophytes with disc space narrowing in each of the five lumbar intervertebral levels.

CE

However, more patterns of osteophytes exist, such as two levels of osteophytes or

AC

those without disc space narrowing. The differences among various patterns should be further investigated. Third, the fibers were assumed to buckle with no change in material properties of the annulus ground substance [11]. Rutges et al. [35] found that calcification was present in degenerated intervertebral discs, thus the material properties of the annulus ground substance may vary in different subjects and this should be further analyzed through in vitro biomechanical tests. Some assumptions 16 / 26

ACCEPTED MANUSCRIPT

were made in the current study. We assumed that the position of nucleus-annulus interface was not changed with osteophyte formation and disc height narrowing. The structure in the intervertebral disc may alter during degeneration. In future studies, confirming the nucleus-annulus interface could more accurately predict the load. The

CR IP T

ligaments were modeled as 1-D connectors in the current study. When focusing on the degeneration effect, future studies could use continuum elements.

AN US

Conclusions

Anterior lumbar vertebral body osteophytes with disc space narrowing influence the kinematics of both the affected and the adjacent levels in the spine. The segments

M

which are close to the osteophytic level may have increased ROM and stress. This study provides insight into the biomechanics of lumbar disc degeneration involving

ED

osteophytes. Further clinical observation should be performed to verify the current

CE

PT

results.

AC

References

[1] Schmorl G, Junghanns H. The Human Spine in Health and Disease (2nd American edition translated and edited by Besemann EF). Grune and Stratton, New York 1971.

[2] Chanapa P, Yoshiyuki T, Mahakkanukrauh P. Distribution and length of osteophytes in the lumbar vertebrae and risk of rupture of abdominal aortic aneurysms: a study of dry bones from Chiang Mai, Thailand. Anat Cell Biol 2014;47:157-61. [3] O'Neill TW, McCloskey EV, Kanis JA, et al. The distribution, determinants, and clinical correlates of vertebral osteophytosis: a population based survey. J Rheumatol 1999;26:842-8. [4] Heggeness MH, Doherty BJ. Morphologic study of lumbar vertebral osteophytes. South Med J 1998;91:187-9. [5] Pye SR, Reid DM, Lunt M, Adams JE, Silman AJ, O'Neill TW. Lumbar disc degeneration: 17 / 26

ACCEPTED MANUSCRIPT

association between osteophytes, end-plate sclerosis and disc space narrowing. Ann Rheum Dis 2007;66:330-3. [6] Wong SH, Chiu KY, Yan CH. Review Article: Osteophytes. J Orthop Surg (Hong Kong) 2016;24:403-10. [7] Macnab I. The traction spur. An indicator of segmental instability. J Bone Joint Surg Am 1971;53:663-70. [8] Lipson SJ, Muir H. Vertebral osteophyte formation in experimental disc degeneration. Morphologic and proteoglycan changes over time. Arthritis Rheum 1980;23:319-24. [9] Kirkaldy-Willis WH, Farfan HF. Instability of the lumbar spine. Clin Orthop Relat Res

CR IP T

1982;(165):110-23.

[10] Al-Rawahi M, Luo J, Pollintine P, Dolan P, Adams MA. Mechanical function of vertebral body osteophytes, as revealed by experiments on cadaveric spines. Spine 2011;36:770-7.

[11] 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 (Bristol, Avon) 2007;22:988-98.

AN US

[12] Nagaraja S, Awada HK, Dreher ML, Gupta S, Miller SW. Vertebroplasty increases compression of adjacent IVDs and vertebrae in osteoporotic spines. Spine J 2013;13:1872-80. [13] Weinhoffer SL, Guyer RD, Herbert M, Griffith SL. Intradiscal pressure measurements above an instrumented fusion. A cadaveric study. Spine 1995;20:526-31.

[14] Chen CS, Cheng CK, Liu CL, Lo WH. Stress analysis of the disc adjacent to interbody fusion in lumbar spine. Med Eng Phys 2001;23:483-91.

[15] Dreischarf M, Zander T, Shirazi-Adl A, et al. Comparison of eight published static finite element J Biomech 2014;47:1757-66.

M

models of the intact lumbar spine: predictive power of models improves when combined together. [16] Panjabi MM, Greenstein G, Duranceau J, Nolte LP. Three-dimensional quantitative morphology

ED

of lumbar spinal ligaments. J Spinal Disord 1991;4:54-62. [17] Xu M, Yang J, Lieberman IH, Haddas R. Lumbar spine finite element model for healthy subjects: development and validation. Comput Methods Biomech Biomed Engin 2017;20:1-15.

PT

[18] Newell N, Little JP, Christou A, Adams MA, Adam CJ, Masouros SD. Biomechanics of the human intervertebral disc: A review of testing techniques and results. J Mech Behav Biomed

CE

Mater 2017;69:420-34.

[19] Schmidt H, Heuer F, Simon U, et al. Application of a new calibration method for a three-dimensional finite element model of a human lumbar annulus fibrosus. Clin Biomech

AC

(Bristol, Avon) 2006;21:337-44.

[20] Rohlmann A, Zander T, 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;39:2484-90.

[21] Naserkhaki S, Jaremko JL, Adeeb S, El-Rich M. On the load-sharing along the ligamentous lumbosacral spine in flexed and extended postures: Finite element study. J Biomech 2016;49:974-82. [22] Schmidt H, Bashkuev M, Dreischarf M, et al. Computational biomechanics of a lumbar motion segment in pure and combined shear loads. J Biomech 2013;46:2513-21. [23] Shirazi-Adl A, Ahmed AM, Shrivastava SC. Mechanical response of a lumbar motion segment in axial torque alone and combined with compression. Spine 1986;11:914-27. 18 / 26

ACCEPTED MANUSCRIPT

[24] Schmidt H, Heuer F, Drumm J, Klezl Z, Claes L, Wilke HJ. Application of a calibration method provides more realistic results for a finite element model of a lumbar spinal segment. Clin Biomech (Bristol, Avon) 2007;22:377-84. [25] Rohlmann A, Neller S, Claes L, Bergmann G, Wilke HJ. Influence of a follower load on intradiscal pressure and intersegmental rotation of the lumbar spine. Spine 2001;26:E557-61. [26] Panjabi MM, Oxland TR, Yamamoto I, Crisco JJ. Mechanical behavior of the human lumbar and lumbosacral spine as shown by three-dimensional load-displacement curves. J Bone Joint Surg Am 1994;76:413-24. [27] Brinckmann P, Grootenboer H. Change of disc height, radial disc bulge, and intradiscal pressure

CR IP T

from discectomy. An in vitro investigation on human lumbar discs. Spine 1991;16:641-6. [28] 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;15:720-30.

[29] Volkheimer D, Galbusera F, Liebsch C, et al. Is intervertebral disc degeneration related to

segmental instability? An evaluation with two different grading systems based on clinical imaging.

AN US

Acta Radiol 2018;59:327-35.

[30] Mimura M, Panjabi MM, Oxland TR, Crisco JJ, Yamamoto I, Vasavada A. Disc degeneration affects the multidirectional flexibility of the lumbar spine. Spine 1994;19:1371-80. [31] Panjabi MM. The stabilizing system of the spine. Part I. Function, dysfunction, adaptation, and enhancement. J Spinal Disord 1992;5:383-9 discussion 397.

[32] Granacher U, Lacroix A, Muehlbauer T, Roettger K, Gollhofer A. Effects of core instability strength training on trunk muscle strength, spinal mobility, dynamic balance and functional

M

mobility in older adults. Gerontology 2013;59:105-13.

[33] Hangai M, Kaneoka K, Kuno S, et al. Factors associated with lumbar intervertebral disc degeneration in the elderly. Spine J 2008;8:732-40.

ED

[34] Zhao F, Pollintine P, Hole BD, Dolan P, Adams MA. Discogenic origins of spinal instability. Spine 2005;30:2621-30.

[35] Rutges JP, Duit RA, Kummer JA, et al. Hypertrophic differentiation and calcification during

AC

CE

PT

intervertebral disc degeneration. Osteoarthritis Cartilage 2010;18:1487-95.

19 / 26

ACCEPTED MANUSCRIPT

Tables Table 1 Material properties of different structures in the finite element model

Cancellous bone

E = 200 MPa, v = 0.25

[21]

Cortical bone

E = 12,000 MPa, v = 0.3

Endplate cartilage

E = 5 MPa, v = 0.17

Annulus ground

Mooney-Rivlin C1 = 0.18, C2 = 0.045

[20]

Annulus fiber

Nonlinear stress-strain curve

[23]

Nucleus

Incompressible, bulk moduls = 2,000 MPa

[19]

[21] [22]

AN US

Disc

References

M

Bone

Material property

CR IP T

Component

Nonlinear force-displacement curve

ED

Ligaments

PT

Table 2 Detailed physiological loading modes applied to L1 vertebra Follower load (N)

Moment (Nm)

Flexion

1175

7.5

500

7.5

Lateral bending

700

7.8

Axial rotation

720

5.5

CE

Body positions

AC

Extension

20 / 26

[19, 24]

ACCEPTED MANUSCRIPT

Figure captions

AC

CE

PT

ED

M

AN US

CR IP T

Fig. 1. Intact lumbar finite element model with no degeneration.

21 / 26

ACCEPTED MANUSCRIPT

Fig. 2. Lumbar finite element model with different degrees of anterior vertebral body osteophytes and disc height narrowing. The mild, moderate and severe grades (grade 1-3) of osteophyte formation were modeled coupled with disc height loss of 16.5%, 49.5% and 82.5%, respectively. The length of osteophytes was modeled to be equal to

AC

CE

PT

ED

M

AN US

CR IP T

the height decrease of the intervertebral space.

22 / 26

ACCEPTED MANUSCRIPT

Fig. 3. Model validation (black dots and red bars show the in vitro median value and

AN US

CR IP T

range of results. The black bars refer to the standard deviations.)

Fig. 4 Validation of segments with anterior vertebral body osteophytes and disc height

M

narrowing. (Intersegmental rotation in lateral bending and axial rotation included both

AC

CE

PT

ED

sides.)

23 / 26

ACCEPTED MANUSCRIPT

Fig. 5. Intersegmental rotation of the lumbar levels with different degrees of anterior

AC

CE

PT

ED

M

AN US

CR IP T

vertebral body osteophytes under physiological loading.

24 / 26

CR IP T

ACCEPTED MANUSCRIPT

Fig. 6. Changes in intersegmental rotation (ISR) of the lumbar levels superior/inferior to the levels with osteophyte formation (OF). “+3, +2, +1, -1, -2, -3” refers to the

AN US

levels higher or lower than the OF level. Note that the changes in ISR of most

AC

CE

PT

ED

M

segments two or three levels inferior to the OF level were almost equal to zero.

25 / 26

ACCEPTED MANUSCRIPT

Fig. 7. Intradiscal pressure (IDP) and maximumvon Mises stress on the annulus ground substance of the levels superior or inferior to the levels with osteophyte formation (OF). “+3, +2, +1, -1, -2, -3” refers to the levels higher or lower than the OF level. Note that the changes in IDP of segments two or three levels inferior to the

AC

CE

PT

ED

M

AN US

CR IP T

OF level were almost equal to zero.

26 / 26