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PII: S0021-9290(17)30361-5
DOI: http://dx.doi.org/10.1016/j.jbiomech.2017.07.002
Reference: BM 8290
Please cite this article as: D.J. Coombs, P.J. Rullkoetter, P.J. Laz, Efficient Probabilistic Finite Element Analysis
of a Lumbar Motion Segment, Journal of Biomechanics (2017), doi: http://dx.doi.org/10.1016/j.jbiomech.
2017.07.002
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An original article
Corresponding Author:
Coombs, Dana J.
DePuy Synthes
1301 Goshen Parkway
West Chester, PA 19380, USA
610-719-6919
dcoombs3@its.jnj.com
Rullkoetter, Paul J.
Center for Orthopaedic Biomechanics
University of Denver
2390 South York Street
Denver, CO 80208
303-871-3512
paul.rullkoetter@du.edu
Laz, Peter J.
Center for Orthopaedic Biomechanics
University of Denver
2390 South York Street
Denver, CO 80208
303-871-3614
peter.laz@du.edu
Keywords: finite element analysis, lumbar, disc, nucleus pulposis, annulus fibrosis,
Holzapfel, Gasser, Ogden, Mooney Rivlin, spinal ligament, calibration, probabilistic,
Monte Carlo, Descriptive sampling, Sobol sampling, functional spinal unit
Page 1 of 30
ABSTRACT
Finite element models of the lumbar spine are useful in assessing biomechanics
and performance of implants. Models are often developed using the anatomy of an
individual subject. Average mechanical property values for the annulus and other soft
tissue structures are typically utilized from the literature, as data for the same subject
are not available. However, these properties can have significant variability. While
probabilistic methods enable the impact of soft tissue property variability on spine
the objective of this study was to develop efficient methods to perform Monte Carlo
variability in the properties of the soft tissue structures. Distributions for the soft tissue
methods, including the Sobol and Descriptive sampling techniques, were assessed for
Comparisons were based on output torque-rotation curves at the 10th and 90th
percentile for flexion, extension, axial rotation, and lateral bending. The Descriptive
sampling technique best matched the random sampling technique, at the extremes of
rotation, with a 3.6% mean difference. This was achieved with a 10X reduction in the
Page 2 of 30
1. INTRODUCTION
repaired spines. Experimental tests provide direct measurements, but are expensive
mechanics (Ayturk et al., 2011; de Visser et al., 2007; Eberlein et al, 2004; Ezquerro et
al., 2004; Ezquerro et al., 2011; Guan et al, 2006; Lu et al., 1996; Schmidt et al., 2007;
Wong et al., 2003). For example, a subject-specific model provides a consistent method
to compare implant performance (Bono et al., 2007; Bowden et al., 2008; Chiang et al.,
2006; Dooris et al., 2001; Goel et al., 2005; Polikeit et al., 2003; Rohlmann et al., 2005;
Tsuang et al., 2009; Vadapalli et al., 2006; Xiao et al., 2012; Zhong et al., 2009). While
both models and experiments assess torque-rotation behavior, some measures can be
extracted from a model that cannot be easily measured experimentally including bone
strain, facet contact force, disc pressure, and annulus fibrosis (AF) strain. Deterministic
models are typically based on anatomy generated from medical image data. In some
cases, the soft tissue representation is based on tissue tests from the same specimen,
but in most cases, the ligaments are defined as the average values reported in the
as distributions and predict output distributions and bounds of performance, while also
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parameters, are most influential. Previous studies have applied Monte Carlo (MC)
the soft tissue properties and anatomy (Lee et al., 2005; Barnes et al., 2011). Modeling
has also considered the failure of a vertebral body based on the variability of stress
measures in the bone (Ahman et al., 2010; Rohlmann et al., 2010). In addition,
probabilistic studies have assessed the mechanics associated with total disc
replacement (TDR) with variability in implant alignment in the disc space and key
(Isight Component Guide, Saliby 1990) and Sobol Sampling (Burhenne et al., 2011, Isight
Component Guide) can predict output distributions with similar accuracy in fewer
2001).
input parameters, and can extend the findings for a few subjects to better represent the
experimental literature and calibrated the material properties for models of tissue-level
ligaments. The objective of this study was to demonstrate efficient methods to perform
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probabilistic predictions of spine mechanics considering variability in the properties of
soft tissue structures using Monte Carlo simulations of a finite element model of the L4
L5 functional spinal unit. Variance reduction sampling methods, including the Sobol and
output torque-rotation curves at the 10th and 90th percentile for flexion, extension,
2. METHODS
Dassault Systemes, Johnston, RI), using an implicit solver, for the L4-L5 FSU from a
healthy 33 year old male with no evidence of disc degeneration (Fig. 1) (Rao, 2012,
Coombs et al., 2013). The vertebral geometry was segmented from a CT scan using
ScanIP (Simpleware, Exeter, UK) and bones were represented by 3-noded triangular
rigid elements (Element type=R3D3). The AF was meshed with 8-noded hexahedral
elements (Element type=C3D8R) and the nucleus pulposis (NP) was represented with an
8-noded fluid-filled membrane (Element type= SFM3D4R). The AF was modeled using
constitutive model. This constitutive model was chosen because the embedded fibers
direction and dispersion, to be modified. The AF was divided into four quadrants
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representing an anterior, posterior, and right and left lateral quadrants due to the
variation in material properties in the AF (Kurtz et al., 2006). The orientation of the
elements in the AF was defined with the normal direction of the outer surface of the
disc as the radial direction, the anatomical inferior/superior axis, and the remaining
tangential direction derived via cross-product. The superior and inferior surfaces of the
disc were kinematically coupled to a reference point at the center of the L4 and L5
vertebral bodies, respectively. Because the vertebrae were defined as rigid, this results
in the same behavior as a tied constraint between the disc surface and the vertebral
endplates. The articulating facet surfaces were rigid and represented by 8-noded
hexahedral elements (Element type=C3D8R) using linear pressure over closure contact
(Rao et al., 2009). Seven passive ligaments were defined in the model using non-linear
tension only connector elements. The ligaments included the anterior longitudinal
intraspinous ligament (ISL), intertransverse ligament (ITL), facet capsular ligament (FCL)
and ligamentum flavum (LFL). The ligament attachment sites were based on dissection
performed after testing and agreed with literature-based descriptions (Panjabi et al.,
1991).
The test frame applied pure moments of 10Nm at the L4 vertebrae while
allowing passive translation at the L5 vertebrae. Rotation was measured using a Vicon
motion capture system (Vicon, Denver, CO). The resulting measurements were 5.92 of
extension, 8.66 of flexion, 6.01 of lateral bending, and 1.75 of axial rotation (Rao,
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2012; Coombs et al., 2013). These rotations were applied to the model and the reaction
comprehensive summary of direct mechanical test data; distributions of stiffness for the
7 spinal ligaments were defined with mean and standard deviation and used as input in
the current study (Table 1). The data compiled were focused at the L4 L5 level;
however, data from other levels were used in cases when the L4 L5 data were not
single stiffness parameter was defined for the stiffness of the linear load displacement
behavior for each ligament. Two inflection points were defined to represent the toe in
region based on the mechanical test data found in literature. The location of the points
Properties for the AF were defined for the four quadrants; anterior, posterior,
and left and right lateral. The left and right lateral quadrants were assumed to be
constitutive model (Holzapfel et al., 2000) to match the distribution found in the
Page 7 of 30
literature summary. The Holzapfel-Gasser-Ogden model is defined by five parameters
C10 affects the stiffness of the ground substance. k1 affects the stiffness of the fibers in
the material. k2 determines the nonlinearity of the fiber stiffness (Abaqus Theory Guide
Chapter 4.6.3, release 6.12). This is a phenomenological constitutive model and the
fiber stiffness values do not represent individual fibers or indicate the number of
discrete fibers. The compressibility parameter, D, was defined as 1/(20*C 10), which is
equivalent to defining the initial bulk modulus as twenty times the initial shear modulus.
Poissons ratio of 0.475 (Abaqus Users Guide Chapter 22.5.1, release 6.12). The fiber
dispersion parameter, , was set to 0 assuming the fibers are perfectly aligned to the
fiber direction. As a result, three input parameters (C10, k1, k2) defined the Holzapfel-
Gasser-Ogden relationship for each quadrant. The best agreement to literature data
parameters. Mean and standard deviations for the parameters are reported for each
An initial assessment of the FE model was performed using mean values of the
soft tissue parameters and compared the torque rotation behavior and range of motion
Page 8 of 30
2.3 Probabilistic Methods
Systemes, Johnston, RI) to determine the uncertainty of the torque-rotation curves for
flexion, extension, axial rotation, and lateral bending based on the uncertainty of the
soft tissue parameters. The random sampling technique with 500 iterations established
the baseline. Sampling error and convergence were calculated to assess the quality of
the predictions. To assess the number of trials required to achieve convergence, the
Monte Carlo simulation was evaluated by calculating the cumulative 10th and 90th
percentile of the reaction moment at the end of the applied rotation and then
calculating the percent error between the current iteration cumulative percentile and
The Descriptive and Sobol variance reduction techniques were evaluated. The
the space defined by each random input parameter is divided into subsets of equal
probability and the analysis is performed with the value for each subset of each random
parameter selected only once. The Sobol sampling technique uses a quasi-random
sequence to generate samples of input parameters more uniformly than random and
Descriptive Sampling while considering previously sampled points to avoid clusters and
gaps (Burhenne et al., 2011). The Sobol sequence generates numbers as binary
fractions of appropriate length from a set of special binary fractions. The Descriptive
Sampling and Sobol Sampling techniques were used with 50 and 25 iterations and
Page 9 of 30
performed for the 10th percentile and 90th percentile torque rotation curves. Error was
computed as the sum of the squared differences in reaction moment between the
efficient prediction and the baseline results established with 500 iterations of random
sampling. The error was calculated using 20 evenly distributed points along the torque-
A sensitivity study was also performed to identify which input parameters most
affected the reaction torque. Initially, the Parameter Study functionality in Isight was
assess its impact on the output. Further, correlations, a measure of sensitivity, were
calculated for the 500 random sampling data points using the Pearson Product-Moment
Correlation Coefficient. Visualizing the sampling data also identified that some of the
relationships between the input parameters and the reaction torques were nonlinear.
3. RESULTS
The FE model with ligament and disc parameters defined at their mean values fit
well within the ranges of motion reported in the literature. Guan et al. (2006) reported
torque rotation curves and their statistics for 10 L4-L5 FSUs (50.6 +/- 13.2 years old,
max 68, min 27) loaded with a pure moment in flexion, extension, lateral bending and
axial rotation. Campbell et al. (2011) reported similar data with 9 L4-L5 FSUs (mean
Page 10 of 30
65.5 years old, max 75, min 48). Qualitatively, the model falls between the
experimental ranges of +/- 1 standard deviation for all degrees of freedom with the
exception of extension. This is also true for the subject specific test data measured from
the specimen that was used to define the anatomy of the FE model (Fig. 2). Symmetric
Total range of motion was also compared at specified moments. Campbell et al.
(2011) also reported range of motion at 10Nm for flexion, extension, lateral bending,
and axial rotation. Yamamoto et al. (1989) reported similar data based on 10 L4-L5
FSUs (25 to 63 years). Panjabi et al. (1994) reported range of motion at 4Nm for
flexion, extension, and lateral bending based on 9 FSUs (35 to 62 years) and Guan et al.
(2006) reported similar data based on 10 L4-L5 FSUs (mean 50.6 +/- 13.2 years). The FE
data was within 1 standard deviation of a literature source for each motion except for
flexion-extension at 10Nm, which was between the mean valued reported by Campbell
et al. (2011) and Yamamoto et al. (1989) (Fig. 3). There was not a literature source to
For all degrees of freedom (flexion, extension, axial rotation, and lateral bend),
torque-rotation curves for the FSU at the 10th and 90th percentiles showed that Monte
Carlo simulations with the Descriptive and Sobol sampling methods compared well with
the baseline random sampling method with 500 iterations (Fig. 4). Results for the
Page 11 of 30
iterations. The sum of the squared error (SSE) quantified differences between the
torque-rotation curves for the various methods (Fig. 4, Table 3). The SSE was lower for
certain methods in specific degrees of freedom (e.g. Sobol with 50 iterations for lateral
bending). The Descriptive sampling technique with 50 iterations had the smallest mean
SSE across all degrees of freedoms (2.74 (Nm)2) and for flexion-extension (1.10 (Nm)2)
Computation time for each iteration was approximately 70 minutes for all
simulation with 500 iterations took 24 days, underscoring the need for more efficient
approaches. The 25 and 50 iteration methods took approximately 1.2 days and 2.4
days, respectively. In Monte Carlo simulation with random sampling, the number of
trials and the location (mean or tail) in the distribution influenced the accuracy of the
results. For 500 iterations, confidence intervals bounding the predictions were
computed for the 10th and 90th percentile torque-rotation curves at the maximum
applied rotation (Table 4) and provide a context for error comparison with the variance
reduction methods (Haldar et al., 2000). The convergence error for flexion, extension,
axial rotation, and lateral bending was less than 0.5% at 500 iterations, which supported
the us the results as the baseline for comparison with the variance reduction sampling
techniques.
Page 12 of 30
The sensitivity analysis identified the key input parameters, and was influenced
by the degree of freedom for the applied rotation (flexion, extension, axial rotation, and
lateral bending) and the relative location/contribution of the soft tissue structures (Fig.
5a). For example, the torque-rotation behavior during flexion was most sensitive to the
stiffness of the SSL and ISL. During extension, the torque-rotation behavior was most
sensitive to the stiffness of the ALL and the C 10 parameter of the anterior disc quadrant.
During lateral bending, the torque-rotation behavior was most sensitive to the stiffness
of the ITL and C10 parameter of the lateral disc quadrant. Input parameters identified
based on correlations from the Monte Carlo simulation generally matched the
parameters from the perturbation study (Fig. 5). However, the fiber angle parameter
had the greatest impact on the torque-rotation behavior for the extension, axial
rotation, and lateral bending rotations. To investigate further, correlations in the input
and output data from the baseline random sampling analysis (500 trials) were computed
and relationships between fiber angle and the reaction torque were investigated. By
plotting the reaction moments as a function of fiber angle (Fig. 6), the point clouds
exhibited trends for extension and axial rotation. For these degrees of freedom, the
moment and a resulting greater sensitivity. The correlations and relationships between
fiber angle and reaction moment were less strong for lateral bending and flexion.
4. DISCUSSION
Page 13 of 30
The aim of this study was to assess whether variance reduction techniques, like
the Descriptive or Sobol sampling, could accurately and more efficiently predict the
Monte Carlo simulation with random sampling. This study focused on the variability in
torque rotation behavior due to variability in the soft tissue representations of the AF
and ligaments. A probabilistic representation from Coombs et al. (2016) established the
distributions from a literature review of direct mechanical test data and FE analyses of
spine uses average values for soft tissue properties. The use of the probabilistic
representation to represent the soft tissue properties in the predictions of the current
study are particularly relevant as they enable consideration of the impact of intersubject
variability.
Baseline in the current study was established with a traditional Monte Carlo
simulation using random sampling with 500 iterations and required approximately 4
days of computation time. Descriptive sampling and Sobol sampling techniques were
shown to reduce the computation time with similar levels of accuracy. The Descriptive
sampling technique with 50 iterations was recommended as the results compared well
to the baseline Monte Carlo simulation (500 trials); the total SSE error was 21.88 (Nm) 2
and required 1.2 days or about a 90% reduction in computation time. A deformable
representation of this model was also run and increased the computation time by 10.
This further demonstrates the need for an efficient sampling method if using a
deformable model.
Page 14 of 30
The probabilistic FE modeling approach uniquely allows investigators to assess
how the experimental variability in small tissue specimens propagates to influence the
mechanics of an FSU or the entire spine. Leveraging the efficient methods, the ability to
motions, can be useful in establishing ranges for healthy normal populations, assessing
pathologies (e.g. disc degeneration) and informing implant design and surgical
other output measures of interest, such as disc pressure, facet contact or annulus strain,
can be similarly assessed. These measures would need to also be compared to physical
biomechanics data.
Using a sensitivity analysis, the most important variables influencing the specific
outputs were identified for each applied rotation. As expected, the reaction moment
was generally most sensitive to ligaments that had the greatest moment arms
considering the direction of the applied motion. This observation was also true for the
quadrants of the AF. Surprisingly, the reaction moments were most sensitive to the AF
fiber angle in the extension and axial rotation degrees of freedom. The distribution for
fiber angle was derived from Guerin et al. (2006) from direct experimental
measurement. This variability was determined from outer anterior annulus specimens
from 8 discs. The reaction moments were not as sensitive at lower values of fiber angles
because the component of the force generated by the fiber angle resisting the rotation
is smaller. This finding underscores the importance of accurately measuring the fiber
angle when performing tests. Further biomechanical studies to better characterize the
Page 15 of 30
variation present in fiber angle and understand the relationship between AF fiber angle
and the torque rotation response are recommended. Further studies should also be
conducted to understand the sensitivity of fiber angle and fiber stiffness in degenerated
and the parameter values reported in this study reproduce the torque-rotation curves.
This material model was defined with initially nearly incompressible behavior. It is
possible that another set of parameter values with a purely incompressible material
would provide similar load displacement behavior, which could decrease the sensitivity
The finite element model utilized in the study was based on the anatomy of a
single specimen (33 years, male, 59 kg). The specimens anatomy was compared to
anatomy data derived from 157 healthy spines with a mean age of 26.8 years (Gilad et
al., 1986). In general, the specimens L4-L5 anatomy was slightly smaller than the
average reported by Gilad et al. (1986). The majority of the measurements were within
1 standard deviation of the mean (Table 5), with the exception of the anterior/posterior
(A/P) width of the superior L5 endplate. The anterior and posterior FE model disc height
was greater than the mean disc height. Therefore, the disc in the FE model was taller
and narrower than the literature means, causing the disc to be more flexible in flexion
and extension. This observation could explain why the model is less stiff with mean
parameter values than the typical torque rotation curves. Furthermore, the donor used
to define the FE model was 177.8cm tall compared to the mean height of 174.7cm from
Page 16 of 30
In this study, the bony anatomy was approximated as a rigid body. As the model
outputs are focused on kinematics and torque-rotation behavior, they should not be
have made similar assumptions (Thacker et al., 2001; Coombs et al. 2013). While
variability in the soft tissue properties was considered, future work could include
variability in the bony anatomy, facet cartilage geometry, and even loading conditions.
population and efficiently generating virtual subjects for finite element analysis
(Hollenbeck et al., 2013). The bony anatomy could also be treated as deformable and
the variability in bone stiffness could be included. This would require significant effort
because the modulus of bone spatially varies and needs to be accurately correlated to
were based on data from a healthy normal population. Further work could be
which may be useful when assessing pathology or developing spinal implants. Studies
have shown that disc degeneration influenced the torque-rotation behavior of the FSU;
range of motion generally decreased with more severe degeneration (Rohlmann et al.,
2006).
probabilistic analyses to be completed in 10% of the time required for the traditional
Page 17 of 30
efficiency enables consideration of the uncertainty present in the population and can be
employed for timely design phase assessments of spinal implant designs and
ACKNOWLEDGEMENT
This study was supported in part by DePuy Synthes. The authors gratefully acknowledge
the model development work performed by Dr. Milind Rao and experimental testing
Page 18 of 30
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CAPTIONS
Figure 1. Finite element model of L4 L5 FSU model with detailed representation of the
disc showing anterior, posterior, and lateral regions of the annulus fibrosis, and a
representative load vs. displacement graph of the ALL with mean and +/- 1 standard
deviation of stiffness.
Figure 3. Total range of motion compared to available literature data at 4Nm and 10Nm
for flexion-extension (FE), lateral bending (LB) and axial rotation (AR) degrees of
freedom. Model predictions are based on average parameter values.
Figure 4. Comparison of torque-rotation behavior for Monte Carlo results at 10th and
90th percentile, using random, Descriptive and Sobol sampling.
Figure 5. Parameter sensitivity assessed via parameter perturbation in Isight (a) and
correlations based on Monte Carlo simulation data (b). Results shown for flexion,
extension, axial rotation and lateral bending reaction moments at the maximum range
of motion.
Figure 6. Scatter plots of annulus fiber angle vs. reaction moments for flexion, extension,
axial rotation and lateral bending with Pearson Correlation Coefficients. Each data point
represents one of the 500 Monte Carlo iterations.
Table 2. Equations for Ligament Load vs. Displacement Behavior, Npar = number of
elements in parallel, Nser = number of elements in series, K = stiffness
Table 3. Sum of squared error (Nm)2 comparison of Descriptive and Sobol sampling to
baseline random sampling (500 trials) for flexion-extension, axial rotation, and lateral
bending degrees of freedom
Table 4. Confidence interval (alpha = 0.95) bounds for the reaction moment (Nm) at the
maximum applied rotation. Calculation is based on traditional random Monte Carlo
sampling with 500 trials.
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Table 5. Comparison of FSU anatomic measurements between specimen/model and
statistical measurements from Gilad et al. (1986).
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Table 1. Summary of input parameters representing ligaments and annulus fibrosis
(Coombs et al., 2016)
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Table 2. Equations for Ligament Load vs. Displacement Behavior, Npar = number of
elements in parallel, Nser = number of elements in series, K = stiffness
ALL
PLL
SLL
LFL
ITL
ISL
FCL
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Table 3. Sum of squared error (Nm)2 comparison of Descriptive and Sobol sampling to
baseline random sampling (500 trials) for flexion-extension, axial rotation, and lateral
bending degrees of freedom.
Axial Lateral
Extension Extension
Rotation Bending Mean
Sampling Percentile Percentile
Percentile Percentile Error
Technique (Nm)2 (Nm)2
(Nm)2 (Nm)2 (Nm)2
10th 90th 10th 90th 10th 90th 10th 90th
Descriptive 2.78
0.09 3.22 0.38 4.81 0.58 10.95 1.93 0.25
25 Iterations
Descriptive 2.74
0.15 1.31 1.88 1.04 4.28 7.98 0.33 4.91
50 Iterations
Sobol 10.10
0.06 6.78 20.07 25.33 2.67 23.48 0.62 1.82
25 Iterations
Sobol 4.77
0.04 8.46 9.18 5.15 0.04 14.16 0.56 0.53
50 Iterations
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Table 4. Confidence interval (alpha = 0.95) bounds for the reaction moment (Nm) at the
maximum applied rotation. Calculation is based on traditional random Monte Carlo
sampling with 500 trials.
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Table 5. Comparison of FSU anatomic measurements between specimen/model and
statistical measurements from Gilad et al. (1986).
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