Original Article

J Appl Biomater Funct Mater 2015 ; 13 (1): 66 -71 DOI: 10.5301/jabfm.5000176

Structural behavior of human lumbar intervertebral disc under direct shear Hendrik Schmidt1,2, Kim Häußler1, Hans-Joachim Wilke1, Uwe Wolfram1,3 Institute of Orthopaedic Research and Biomechanics, University of Ulm, Ulm - Germany Julius Wolff Institut, Charité – Universitätsmedizin Berlin, Berlin - Germany 3 Institute for Surgical Technology and Biomechanics, University of Bern, Bern - Switzerland 1 2

ABSTRACT Purpose: The intervertebral disc (IVD) is a complex, flexible joint between adjacent vertebral bodies that provides load transmission while permitting movements of the spinal column. Finite element models can be used to help clarify why and how IVDs fail or degenerate. To do so, it is of importance to validate those models against controllable experiments. Due to missing experimental data, shear properties are not used thus far in validating finite element models. This study aimed to investigate the structural shear properties of human lumbar IVDs in posteroanterior (PA) and laterolateral (LL) loading directions. Methods: Fourteen lumbar IVDs (median age: 49 years) underwent direct shear in PA and LL loading directions. A custombuild shear device was used in combination with a materials testing machine to load the specimens until failure. Shear stiffness, ultimate shear force and displacement, and work to failure were determined. Results: Each specimen was tested until complete or partial disruption. Median stiffness in PA direction was 490 N/mm and in LL direction 568 N/mm. Median ultimate shear force in the PA direction was 2,877 N and in the LL direction 3,199 N. Work to failure was 12 Nm in the PA and 9 Nm in the LL direction. Conclusions: This study was an experiment to subject IVDs to direct shear. The results could help us to understand the structure and function of IVDs with regard to mechanical spinal stability, and they can be used to validate finite element models of the IVD. Key words: Failure, Finite element method, Intervertebral disc, Shear stiffness, Shear strength Accepted: April 26, 2013

INTRODUCTION The intervertebral disc (IVD) is a complex structure that serves as a strong, flexible joint between adjacent vertebral bodies. It is responsible for transmitting loads in multiple directions while permitting movements of the spine. During certain movements, the disc is at risk of injuries, of which disc prolapses, endplate failures and interlaminar tearing are probably the most significant. To investigate injury, degeneration or trauma of the IVD due to complex loading, finite element (FE) models can be used. FE models of multiple spinal segments often use muscle forces (1) or alternatively the follower load technique (2, 3) for stabilization and the application of physiological loads. To optimize muscle activation or the paths of the follower load, rotations due to bending are minimized so that the disc is loaded in pure compression. An alternative criterion to optimize muscle activation or the path of the follower load could be to minimize the resulting shear forces in a functional spinal unit. This 66

is reasonable because shear forces are directly linked to back injuries (4, 5). The authors assume that the musculoskeletal system of the healthy spine is designed to compensate for shear forces by muscle activation to prevent injuries. Considering such a criterion in a FE model, however, necessitates validation steps in which the model output will be compared with independent data. To do so, structural parameters such as shear stiffness, ultimate load, ultimate elongation and work to failure under prescribed loading conditions are required. The shear force in this context is defined as force acting in the midtransverse plane of the IVD. Few data are presently available to describe the resistances of the IVD to shear. Most of the experimental work on the shear properties of the spine in vitro have focused on the coupled shear motion accompanying flexion– extension (6, 7). The function of the individual spinal structures with respect to shear was investigated by comparing intact specimens against those without posterior elements (8, 9). The authors concluded that the disc accounted for

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Schmidt et al

Fig. 1 - The arrangement for shear loading using an electromechanical material testing machine (Z010; Zwick GmbH & Co. KG, Ulm, Germany). The balance weight ensures that the loading head does not exert additional force on the sample. The upper right sketch illustrates the specimen preparation used for applying direct shear. The lower right diagram shows a representative force–displacement curve. Stiffness (ΔN/Δmm) was determined by a moving regression in the linear region. Ultimate shear force and displacement was the maximum force (Fmax ) and the respective displacement (umax ). The work to failure (W) was determined by integration of the loaddisplacement curve until Fmax. PMMA = polymethylmethacrylate.

approximately 85% of the average stiffness to failure and 74% of the ultimate load. These studies, however, were performed on porcine and rhesus monkey specimens. Pure, nondestructive shearing has been investigated in a study that indicated that motion segments can passively resist 500 N in shear, with shear stiffness ranging from 53 to 140 N/mm (10). In fact, the applied load was a combination of shear and moments, since the forces were applied on average 35 mm above the center of the superior vertebral body. This bending moment can be minimized by applying shear forces at the level of the disc (11, 12). These experiments, however, were performed on the whole spinal segment with intact posterior structures. For isolated IVDs loaded in the posteroanterior (PA) direction, a shear stiffness of 135 N/mm was found for shear loads up to 0-250 N (13). Shear data capturing the entire load range up to failure are currently missing. Furthermore, no data exist for the laterolateral (LL) direction. Shear in this direction can be generated by pure axial rotation due to a center of rotation which is located in the area of the facet joints (14). Therefore, the goal of the current study was to investigate the structural properties of human lumbar IVDs, in terms of stiffness, ultimate force and displacement, and work to failure under direct shear in PA and LL directions. Thereby, it was essential that the boundary and loading conditions of the experimental setup are easily implementable into FE models to directly compare the measurements with the model predictions.

MATERIALS AND METHODS The study complied with the World Medical Association Declaration of Helsinki regarding ethical conduct of research involving human subjects. Permission of the ethical board of Ulm University was granted. Specimen preparation Fourteen lumbar spinal motion segments (L2-L3, L4-L5) were harvested from fresh-frozen human donor spines (median age 50 years; range 20-58 years) and inspected visually and radiographically to exclude spinal diseases, damage and severe degeneration. Specimens were stored at -20°C and thawed for 16 hours at 8°C prior to testing. Surrounding soft tissues, posterior bony structures and all ligaments, except the anterior and posterior longitudinal ligaments, were removed so that the isolated IVDs were preserved. The IVDs were horizontally aligned, and the cranial end of the upper vertebra and the caudal end of the lower vertebra were embedded in polymethylmethacrylate (PMMA) (Technovit 3040; Heraeus Kulzer, Werheim, Germany). Additionally, screws were drilled into the vertebral bodies prior to potting in order to provide a better fixation in the PMMA. A shear gap of 0.5 mm between the 2 molds was set up (Fig. 1). The moulds closely embed the discs so that the disc material can only deform within the 0.5-mm gap. This setup allows

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Intervertebral disc under direct shear

Fig. 2 - Force–displacement curve for all tested intervertebral discs (IVDs) for laterolateral (LL) (a) and posteroanterior (PA) shear (b). Arrow indicates a sudden small stiffness decrease of the IVDs, possibly caused by micro fractures of fibrous structures within the disc.

the application of shear loads by keeping additional moments, tensile or compressive forces as small as possible. Before testing, each specimen was rehydrated in 0.9% saline for approximately 2 hours. The IVDs were kept moist with 0.9% saline throughout the entire experiment. Flanges were fixed to the upper and lower PMMA blocks to mount the specimens in the different testing devices. Experimental protocol The shear test was carried out using a custom-made shearing device (Fig. 1) mounted on an electromechanical materials testing machine (Z010; Zwick GmbH & Co. KG, Ulm, Germany). The embedded segment was clamped tightly within the fixtures by 4 screws at each end to block displacement. The specimens were loaded up to failure. Most of the existing FE models are based on structural quasi-static model responses. Since the shear data should be used in such models, a moderate loading rate of 5 mm/min was used (15). The tests were stopped after the force dropped to 60% of the maximum load. Force and displacement were recorded and digitized at 50 Hz. Seven specimens underwent shear loading in the PA and LL directions. Data analysis Ultimate shear force (Fmax) and the respective displacement (umax) were determined from the force– displacement curve (Fig. 1). The average shear stiffness of the segments was calculated from the load–displacement curve using a moving regression that identified the highest stiffness (16). Work to failure was determined from the beginning of the load–displacement curve until the ultimate point was reached using the trapezoidal quadrature rule (17). For comparison with data from the literature (13), shear stiffness was additionally determined for a force range of 0-250 N by linear regression analysis of the PA and LL shear load–deformation curve. 68

RESULTS Each specimen was tested until complete or partial disruption of the IVD. The load–deformation curves of all tested IVDs showed a nonlinear response characterized by a progressive increase at the beginning of loading, a linear region where the disc stiffness was determined and a declining region until failure (Fig. 2). Inspection of force–displacement curves showed in some cases sudden small oscillations which may have been caused by micro fractures of fibrous structures in the annulus fibrosus (arrow in Fig. 2b). Each oscillation is followed by an irreversible decrease of the slope of the curve. The slope of the loop indicated by the arrow, e.g., decreased by 25 N/mm after the first and 40 N/mm after the second oscillation. The median ultimate shear force was slightly higher in the LL (median: 3,199 N) than in the PA (median: 2,877 N) direction (Fig. 3a). The shear stiffness of the IVDs was also found to be slightly higher in the LL (median: 568 N/mm) than in the PA (median: 490 N/mm) direction (Fig. 3d). In contrast, work to failure was slightly higher in the PA (median: 12.3 Nm) than in the LL (median: 9.1 Nm) direction (Fig. 3c). The median displacement for both loading directions was 9.1 mm and, thus, correct (Fig. 3b). The shear stiffness, which was determined by linear regression analysis of the shear load–deformation curves, was found to be 136 N/mm in the LL direction and 110 N/mm in the PA direction. The latter was comparable to the value found by Lu et al (13), which was 135 N/mm. The number of specimens was too small to derive statistically meaningful conclusions for this segment-wise comparison. The individual results of all tested IVDs are summarized in Table I. DISCUSSION The aim of the resent study was to investigate the structural properties of the human lumbar IVD under direct shear loading. Therefore, ultimate shear force and displacement, shear stiffness and work to failure in the PA and LL directions were analyzed.

© 2014 Società Italiana Biomateriali - eISSN 2280-8000

Schmidt et al

Fig. 3 - Median (whiskers show minimum and maximum) in laterolateral and posteroanterior direction of ultimate shear force to failure (a), displacement umax at the instant of ultimate shear force (b), work to failure (c) and shear stiffness (d). For comparison, disc shear stiffness data for the posteroanterior direction from Lu et al (13) are also shown.

TABLE I - AGE, SEX, SPINAL LEVEL, SHEAR STIFFNESS, ULTIMATE SHEAR FORCE TO FAILURE, DISPLACEMENT AT INSTANT OF ULTIMATE SHEAR FORCE AND WORK TO FAILURE, FOR ALL TESTED INTERVERTEBRAL DISCS AND FOR BOTH TESTING DIRECTIONS Lateral shear Specimen no.

Age

Sex

Level

Stiffness (N/mm)

Ultimate force (N)

Ultimate displacement (mm)

Work to failure (Nm)

1

56

m

L4-L5

389.8

1,743

9.2

8.3

2

49

f

L2-L3

618.9

1,732

5.0

7.6

3

29

m

L4-L5

550.3

3,078

10.6

15.8

4

56

m

L2-L3

582.6

2,876

14.5

10.2

5

29

m

L2-L3

582.8

3,308

10.5

18.3

6

28

f

L4-L5

991.9

3,990

5.8

9.8

7

56

m

L2-L3

555.0

2,048

8.9

11.1

Median

48

567.6

2,877

9.1

9.1

Min

28

389.9

1,732

5.0

7.6

Max

56

991.9

3,990

14.5

18.3

Anterior shear 1

51

m

L2-L3

459.9

2,666

12.2

17.9

2

53

f

L4-L5

413.4

2,081

9.1

8.2

3

56

m

L4-L5

503.3

3,199

10.3

16.7

4

20

m

L2-L3

490.1

1,959

8.1

9.5

5

28

f

L2-L3

812.2

3,512

9.08

17.5

6

46

m

L4-L5

381.9

2,132

10.7

12.3

7

58

f

L2-L3

695.2

3,354

8.2

11.4

Median

51

490.3

3,199

9.1

12.3

Min

20

381.9

2,089

8.1

8.2

Max

58

812.2

5,815

12.2

17.9

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Intervertebral disc under direct shear

The shear forces generated in vivo in the human lumbar spine have been estimated to be in the range of 400 to 800 N (18-21). Shear loads are greatly reduced by the musculature, resulting in approximately 200 N acting in the osteoligamentous spine. In comparison with our findings, this value does not appear to be critical for the disc. However, in case of a spondylolysis, 800 N and higher shear forces may act in the IVD. Thus, shear loads are important to understand disc failure. Analysis of the findings presented here suggests shear strengths well within the upper range of in vivo loads (Fig. 2; Tab. I). For shear forces up to 250 N, the stiffness in the PA direction was comparable to that found in the in vitro experiments of Lu et al (13). That study and the current one observed an almost linear displacement response for shear forces up to 250 N. The authors assume that the collagen fibers are not active under these small loads. However, with increasing shear load, the disc exhibits a stiffening effect resulting in a nonlinear force–displacement response (Fig. 2). This may be due to the increasing resistance of collagen fibers when stretched. The boundary conditions applied in the experimental setup led to direct shear loading in the mid-plane of the IVD by minimizing additional bending moments at the same time. This was realized by a small shear gap of 0.5 mm (Fig. 1). The molds closely embed the discs so that the disc tissue can only deform within the small gap. In comparison with the height of the disc, which is about 11 mm, the gap can be neglected. If the gap had been larger then bending would have been superimposed on normal loads. Thus, leading to a bias in the experiment. The small gap size should have ensured that the disc only deformed in the given plane. Furthermore, the applied load case was well controlled and was therefore directly applicable for comparison in numerical models. If the shear properties of the IVD in numerical models fits the properties in in vitro experiments, this load case can be used as an additional optimization criterion for muscle activation or the follower load description in FE models. The experimental setup allowed only pure shear under small deformations. When the specimens are loaded up to failure, they are subjected to large deformations which result in a combination of shear and normal stresses. Therefore, the presented ultimate shear force includes load combinations which differ from pure shear. However, since the boundary and loading conditions were enforced,

the results are still valuable for validating FE models. Applying similar boundary conditions and taking the load combinations into account, a model to be validated must reflect the resulting ultimate forces and displacements. In the current study, the experiments were performed on specimens which were already subjected to cyclic loads. In a former experiment, specimens were loaded for 50,000 cycles at 5 Hz (Instron 8871; Instron Wolpert GmbH, Darmstadt, Germany) with an eccentric load (lever arm of 30 mm) and an amplitude between 100 and 600 N. During testing, the specimens revolved clockwise on their axis at 360°/min allowing the application of load combinations, beginning from flexion and passing into lateral bending to the right, then into extension and into lateral bending to the left, and starting again in flexion. As presented here, the shear stiffness in the PA direction under relatively small loads was comparable to the published data of Lu et al (13). This is an indicator that the previous cyclic loading did not significantly alter the material and structural properties of the disc, at least with respect to shear loads. If the previous cyclic tests had had an influence on the mechanical behavior under shear, it should have been noticeable in particular under small loads with an increase in laxity and a decrease in stiffness. Given the good comparability in the low load range to the data of Lu et al (13), we think that the results found here are reasonable. However, based on the experiments presented, we are not able to quantify the influence of the previous cyclic test in more detail. This study was an experiment to subject IVDs to direct shear. The results could help us to understand the structure and function of IVDs with regard to their mechanical spinal stability. Furthermore, the results provide data that can be used to validate FE models of the IVD.

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Financial support: This study was supported by the Deutsche Forschungsgemeinschaft (WI 1352/14-1). Conflict of interest: The authors have no conflicts of interest. Address for correspondence: Hendrik Schmidt, PhD Julius Wolff Institut Charité - Universitätsmedizin Berlin CVK; Institutsgebäude Süd / Südstraße 2 Augustenburger Platz 1 DE-13353 Berlin, Germany [email protected]

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Structural behavior of human lumbar intervertebral disc under direct shear.

The intervertebral disc (IVD) is a complex, flexible joint between adjacent vertebral bodies that provides load transmission while permitting movement...
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