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Biomech Model Mechanobiol

DOI 10.1007/s10237-015-0656-2

ORIGINAL PAPER

A forward dynamics simulation of human lumbar spine flexion


predicting the load sharing of intervertebral discs, ligaments,
and muscles
T. K. Rupp W. Ehlers N. Karajan M. Gnther
S. Schmitt

Received: 29 July 2014 / Accepted: 22 January 2015


Springer-Verlag Berlin Heidelberg 2015

Abstract Determining the internal dynamics of the human nonlinearly. As results, internal kinematics, muscle forces,
spines biological structure is one essential step that allows and internal loads for each biological structure are presented.
enhanced understanding of spinal degeneration processes. A comparison between the nonlinear (new, enhanced mod-
The unavailability of internal load figures in other methods elling approach) and linear (standard modelling approach,
highlights the importance of the forward dynamics approach bushing) modelling approaches of the intervertebral disc is
as the most powerful approach to examine the internal degen- presented. The model is available to all researchers as ready-
eration of spinal structures. Consequently, a forward dynam- to-use C/C++ code within our in-house multi-body simula-
ics full-body model of the human body with a detailed lumbar tion code demoa with all relevant binaries included.
spine is introduced. The aim was to determine the internal
dynamics and the contribution of different spinal structures to Keywords Biomechanics Direct dynamics Multi-body
loading. The multi-body model consists of the lower extrem- model Impact Shock wave Computer simulation
ities, two feet, shanks and thighs, the pelvis, five lumbar ver-
tebrae, and a lumped upper body including the head and both
arms. All segments are modelled as rigid bodies. 202 muscles Abbreviations
(legs, back, abdomen) are included as Hill-type elements. 58
nonlinear force elements are included to represent all spinal IVD Intervertebral disc
ligaments. The lumbar intervertebral discs were modelled MTC Muscletendon complex
MB Multi-body
T. K. Rupp M. Gnther S. Schmitt (B) FE Finite element
Institute of Sports and Movement Science, University of Stuttgart, DOF Degree of freedom
Allmandring 28, 70569 Stuttgart, Germany
CT Computed tomography
e-mail: schmitt@inspo.uni-stuttgart.de
URL: http://www.inspo.uni-stuttgart.de/aVI CE Contractile element
IVFE Intervertebral flexionextension
T. K. Rupp W. Ehlers N. Karajan S. Schmitt ROM Range of motion
Cluster of Excellence for Simulation Technology (SimTech),
University of Stuttgart, Pfaffenwaldring 5a,
ALL Anterior longitudinal ligament
70569 Stuttgart, Germany PLL Posterior longitudinal ligament
URL: http://www.simtech.uni-stuttgart.de LF Ligamentum flavum
SSL Supraspinal ligament
W. Ehlers N. Karajan
Institute of Applied Mechanics (Civil Engineering), University
ISL Interspinal ligament
of Stuttgart, Pfaffenwaldring 7, 70569 Stuttgart, Germany RA Rectus abdominis muscle
URL: http://www.mechbau.uni-stuttgart.de/ls2 EO External oblique muscle
IO Internal oblique muscle
N. Karajan
DYNAmore GmbH - Gesellschaft fr FEM Ingenieurdienstleistungen,
PM Psoas major muscle
Headquarter, Industriestr. 2, 70569 Stuttgart, Germany MF Multifidus
URL: http://www.dynamore.de IT_m Intertransversarii mediales

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T. K. Rupp et al.

LTpL Longissimus thoracis pars lumborum et al. 2009), thereby adequate boundary conditions for vari-
IL Iliocostalis lumborum pars lumborum ous life situations (daily activity, physical training, or acci-
C1C7 Cervical vertebrae dental movements) are indispensable for FE analyses in an
T1T12 Thoracic vertebrae accurate and physiologically valid manner. Yet, in vivo mea-
L1L5 Lumbar vertebrae surements for determining, for instance, forces and moments
S1S5 Sacral vertebrae acting on the intervertebral discs or forces on vertebral end-
Sagittal axis Dorsal to ventral (= x-axis) plates as boundary conditions for FE models, have remained
Longitudinal axis Caudal to cranial (= z-axis) extremely challenging. They have not yet been determined in
Graphic primitive Geometric primitive, describes the a satisfactory manner (Rohlmann et al. 2009; Schmidt et al.
simplest geometric objects that the 2010).
system can handle; in this model, the Musculoskeletal MB models of the spine have been devel-
graphic primitives represent respec- oped and used on a larger spatial scale to determine spinal
tive body segments kinematics and loads as well as muscle activation patterns
(de Zee et al. 2007; Stokes and Gardner-Morse 1995). In this
regard, several musculoskeletal MB models of the spine have
1 Introduction been introduced (Cholewicki and McGill 1996; Christophy
et al. 2011; McGill and Norman 1987), thereby challenges
Humans everyday lives lead to frequent impacts on the loco- have arisen due to intersubject variability concerning anthro-
motor system. Over time, this causes natural degeneration of pometry, modelling of joints, intervertebral discs, facet joints,
its biological structures, e. g. bones, muscles, and ligaments. passive ligamentous structures, and active MTCs. Lately,
When focussing on the human lumbar spine, degradation of spinal MB models have shown an increasing level of preci-
the intervertebral discs (IVDs) and the vertebral bodies is sion and complexity. To date, the inverse dynamics approach,
the prominent feature of this process (Cassinelli and Kang cf. Otten (2003), has been mainly used.
2000; Elias 1958; Miller et al. 1988; Sarzi-Puttini et al. 2004; In general, MB models have provided indispensable
Whatley and Wen 2012). Yet, cause and effect of biological options for scientific research to synthesise human movement
degeneration across the lifespan are still under debate. (Gnther and Ruder 2003; Hatze 1976, 1981; Pandy et al.
The evaluation of acting forces and moments within bio- 1990; Soest et al. 2003; Van Soest and Bobbert 1993). How-
logical structures while performing dynamic movement can ever, drawbacks remain when MB models are applied to the
help in gaining more insight into the mechanisms of natural biomechanical analysis of the human spine. Model simplifi-
degeneration. In vitro and in vivo measurements have been cations (e. g. model characteristics of structural elements and
accompanied by computer simulations (in silico) in order to lumped modelling of biological structures) restrict detailed
determine the internal dynamics of the spine. In contrast to biomechanical analyses of the human spine. Lumped mod-
experimental testing, computer models allow biomechanical elling is often found in intervertebral joints, when the IVD,
analyses of the spine in a more efficient, ethically acceptable its surrounding muscles, and ligaments are modelled as one
and completely reproducible manner (Esat and Acar 2008; structural elements (often called bushing element). This way,
Gatton et al. 2011). To achieve this, all relevant structural ele- it is not possible to investigate different structural elements
ments, e. g. vertebrae, IVDs, spinal ligaments, and muscle of the spine, e. g. their force contribution, functionality, and
tendon complexes (MTCs); their material properties; and an purpose, and to assign different features to the involved bio-
appropriate verification of the whole model need to be taken logical structures. Furthermore, it can be stated that so far
into account to accurately predict the internal dynamics and the linear approach has mainly been used for modelling the
the load distribution of the spine, and to analyse the func- structural elements of the spine, e. g. linear bushing element
tionality and purpose of the different biological structures. (Christophy et al. 2011; de Zee et al. 2007). This is in con-
Two different modelling and computer simulation trast to the nonlinear nature of most biological, structural
approaches are commonly used for the mechanical analyses elements, e. g. nonlinear forcelength characteristics.
of the spine: multi-body (MB) simulations and simulations In the presented work, a forward dynamics full human MB
based on the finite-element (FE) method. model with a detailed lumbar spine is introduced. The aim
On a smaller spatial scale, FE models have been used for was to investigate the impact of different structural elements
the calculation of internal stresses in vertebral bodies and on spinal dynamics and the internal loads of spinal struc-
IVDs (Ehlers et al. 2008; Schmidt et al. 2007, 2010), and for tures. Consequently, all load-bearing structures, i.e. muscles,
virtual prototyping and testing of spinal implants (Rohlmann ligaments, and IVDs, were incorporated as separate struc-
et al. 2010). FE models have reached high levels of preci- tures into the MB model of the spine. Internal kinematics
sion when applied to individual organs, i.e. simulation results and the load contribution of different biological structures
closely match with in vitro experimental testing (Rohlmann were analysed. This allows to synthesise spinal movement

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A forward dynamics simulation of human lumbar spine flexion

and to better understand the mechanical degeneration on the method uses a homogeneous matrix transformation approach
spine. As a consequence, it will be possible to investigate the proposed by Denavit et al. (1965), Denavit and Hartenberg
mechanical consequences of daily life and spinal pathologies (1955). It was extended by Legnani et al. (1996a, b) with
to evaluate different surgery methods and physical therapies, the introduction of new homogeneous matrices to describe
as well as to numerically test spinal implants in an accurate the velocity and the acceleration, the momentum, the iner-
and physiologically valid manner. We provide the MB model tia of bodies, and the actions (forces and moments) applied
implemented in C/C++ and the binaries needed for our in- to them, both translational and rotational. The method is
house MB simulation code demoa as electronic supplemen- embraced and implemented in SpaceLib , a library for
tary material and hope that this facilitates the biomechanical three-dimensional dynamics of rigid body systems, that was
research on spinal dynamics. used in demoa (see provided C/C++ code and Henze (2002),
Schmitt (2003) for a detailed description of the mathematical
formulation and usage within demoa).
2 Material and methods
2.1 Model geometry
A full human MB model with a detailed lumbar spine was
developed. The model is driven by the stimulation of muscles. Our spine model consists of seven rigid segments: the pelvis,
Back muscles in the lumbar region, abdominal muscles, and the five lumbar vertebrae, and a lumped thoraciccervic
leg muscles were modelled as Hill-type muscles (Gnther headarms part (upper body, compare Fig. 9). To the best of
et al. 2007; Mrl et al. 2012; Schmitt et al. 2012). Nonlin- our knowledge, a complete anthropometric data set for the
ear ligaments were included in the lumbar spine. The leg cervical, thoracic, and lumbar spine has not been realised yet.
segments (feet, shanks, thighs) were connected to each other A scalable anthropometric data set was generated for the
and the pelvis segment by hinge joints. Adjacent vertebrae as spinal column on the basis of the literature data, i.e. verte-
well as L5 and the pelvis were connected to each other by free bral width and depth (cf. Gilad and Nissan 1986; Panjabi
joints (6 degrees of freedom (DOF)) equipped with IVD force et al. 1992, 1991; White and Panjabi 1990) as well as height
elements. Currently, the full human model has 42 (6 hinge, (cf. Busscher et al. (2010); Gilad and Nissan (1986)), ori-
6 free joints) mechanical DOFs and 404 additional DOFs in entation, and position (cf. Ashton-Miller and Schultz 1997;
the 202 (70 leg, 84 lumbar spine, 48 abdomen) MTCs. Belytschko 1978; El-Rich and Shirazi-Adl 2004; Kitazaki
Modelling and simulation was done with the authors in- and Griffin 1997) of vertebrae. The geometry is assumed to
house MB simulation code demoa, cf. Henze (2002), Schmitt be symmetrical with respect to the sagittal plane (xz-plane).
(2003). Demoa includes the biomechanical preprocessor cal- The global origin of the model is located in between the two
cman, the simulation framework sim, and the animation tool feet on the ground. The local coordinate system of the body
ani. S1 drops perpendicular through the global origin of the whole
Calcman has been developed to calculate subject-derived model. The frontal axis in sagittal plane is defined from dor-
anthropometric data sets. These are used as an input and basis sal to ventral. It is equal to the x-axis. The longitudinal axis
for human MB models. The calculated data sets are based on is defined from caudal to cranial and is equal to the z-axis.
statistical anthropometric data sets from the literature (DIN The generated data set includes position and orientation data
1986; NASA 1978). Calcman uses three input parameters for the lumbar and thoracic spine from S1 to T1 and vertebral
(mass, sex, and height) to calculate a subject-derived anthro- dimensions for all vertebrae from S1 to C3. The generation
pometric data set. Each data set consists of segment para- of the anthropometric data set is explained in Appendix 1.
meters defining the model segments (bodies): length, mass, Position data and orientation angles of each vertebra for
moment of inertia, position, and orientation of its centre of the modelled subject, i.e. a male subject with mass m = 68kg
gravity and joint centre, as well as width, depth, and circum- and height h = 1.78 m, are depicted in Table 1.
ference. Calcman writes the respective kinematic chain as In contrast to the lumbar vertebrae, vertebrae of the tho-
an output. In this work, calcman was extended to generate a racic and cervical spine were not included as single segments
subject-derived geometrical data set of the lumbar spine and in our MB model. Instead, they were merged into the so-
torso (see Sect. 2.1). called upper body representing the head, the upper arms, the
In addition to the geometrical model, (visco-)elastic char- forearms, and the hands as well as the thoracic and the cervi-
acteristics of biological tissue, as for example ligaments or cal vertebrae plus their surrounding soft tissue. The lumped
external contacts, are described and modelled as force ele- upper body mass was included as one point mass positioned
ments, acting on the geometry. in the upper bodys centre of mass, cf. Calisse et al. (1999).
Simulations are performed using sim. The mechanics The centre of mass of the upper body was determined on the
in sim is based on a derivation-free formulation of the basis of the torsos centre of mass (NASA 1978). The NASA
Lagrangian equations in generalised coordinates. This (1978) defines the position of the torsos centre of mass in

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T. K. Rupp et al.

Table 1 Position and orientation data of each vertebra (centre) for the modelled subject, i.e. a male subject with mass m = 68 kg and height
h = 1.78 m, with respect to the global reference frame (origin between feet, vertical line passing through origin and S1)
Level x (mm) z (m) centre ( ) upper ( ) Level x (mm) z (m) centre ( ) upper ( )

T1 40.20 1.48 23.75 26.8 T10 5.33 1.27 2.57 0.4


T2 31.23 1.46 21.67 26.7 T11 3.19 1.24 5.60 5.6
T3 23.48 1.44 19.92 23.9 T12 0.48 1.21 7.37 9.4
T4 15.93 1.42 17.91 19.9 L1 4.93 1.18 7.04 10.0
T5 9.19 1.39 15.54 15.5 L2 8.64 1.14 3.76 3.8
T6 3.20 1.37 12.53 15.5 L3 9.13 1.10 2.89 0.9
T7 1.29 1.35 9.07 14.1 L4 4.16 1.06 11.71 11.7
T8 4.30 1.32 5.31 10.3 L5 6.16 1.03 18.68 18.7
T9 5.77 1.30 1.21 4.2 S1 0.00 0.95  36.0
The x-value on the frontal axis is calculated using Eq. (2), i.e. its value is determined with respect to the vertebraes position on the longitudinal axis
(z). centre is the orientation angle, i.e. inclination angle of the centre of the vertebral body with the frontal (x). upper is the estimated orientation of
the upper endplate with the sagittal axis. Note that vertebral body S1 does not allow to choose a centre lines orientation due to the fusion of the Os
sacrums bones ()

relation to the waist depth and breadth at omphalion and found in Appendix 4. The nonlinear IVD model consists of
the distance between suprasternale and trochanterion. This a third-order polynomial for each DOF to capture the elastic
point was localised in the presented model, and the upper mechanical response of each lumbar IVD, viz.
bodys mass was calculated. The centre of mass of the upper
FIVD-nl,x = 14.548 Nm3 r x3 + 0.4186 Nm2 r x2
body was determined to be positioned 15.1 mm anterior and
6.8 mm cranial to the centre of thoracic vertebra T12 with a + 43.764 Nm1 r x ,
mass of 36.8 kg. FIVD-nl,y = 14.548 Nm3 r y3 0.4186 Nm2 r y2
+ 43.764 Nm1 r y ,
2.2 The spinal ligaments FIVD-nl,z = 32.432 Nm3 r z3 65.925 Nm2 r z2
+ 380.96 Nm1 r z ,
Five spinal ligaments, i.e. anterior longitudinal (ALL) and
posterior longitudinal ligament (PLL), ligamentum flavum MIVD-nl,x = 1.6 Nm/deg x ,
(LF), supraspinal (SSL), and interspinal (ISL) ligament, MIVD-nl,y = 0.0046 Nm/deg3 y3 0.0001 Nm/deg2
were included as nonlinear model elements at each spinal y2 + 1.0158 Nm/deg1 y ,
level between S1 and L1. The developed nonlinear ligament
MIVD-nl,z = 6.9 Nm/deg z , (1)
model and parameter estimation are described in detail in
Appendix 2. with r x displacement in the direction of the frontal joint axis,
Attachment points for the four lumbar ligaments were r y displacement in the direction of the transverse joint axis,
defined in analogy to Panjabi et al. (1982), Pintar et al. (1992). r z displacement in the direction of the longitudinal joint axis,
Proposed anatomical landmarks were identified on the fitted x angle around the frontal joint axis, y angle around the
graphic primitives from CT data (Anatomium (TM), 21st transverse joint axis, z angle around the longitudinal joint
Century Solutions Ltd/Gibraltar). Additionally, ALL, LF, axis.
and ISL were approximated by multiple lines for one liga- Damping forces of the IVD elements were modelled ana-
ment (multiple ligament parts). PLL and SSL were modelled log to damping forces of ligaments (see Sect. 2.2). Linear
by one single line. stiffness parameters were taken from other multi-body mod-
The parameters FA , lA , FB , lB , lLIG,0 , ULIG,nll , ULIG,l , els (Huynh et al. 2010; Monteiro 2009) and one experimen-
FLIG,0 , LIG,nll , and pre-strain data of the included spinal tal data set in its non-coupled version (Gardner-Morse and
ligaments are depicted in Table 5 (Appendix 3). Stokes 2004). They were used to implement linear IVDs for
comparison with our new nonlinear IVD model. The linear
2.3 Joints and the nonlinear intervertebral disc model stiffness parameters are listed in Table 2.
2.4 The abdominal and lumbar back muscles
Human vertebrae are connected by IVDs that allow each
vertebra to move in six DOFs. A detailed description of the The incorporation of the muscle groups into the lumbar spine
development of the nonlinear IVD model used here can be model is depicted in Fig. 1.

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A forward dynamics simulation of human lumbar spine flexion

Table 2 Stiffness parameters for rotational and translational movement of IVDs extracted from linear IVD models
Stiffness parameters Huynh et al. (2010) Monteiro (2009) Gardner-Morse and Stokes (2004)

Anterior shear (N/m) 150,000.0 260,000.0 57,730.0


Lateral shear (N/m) 150,000.0 260,000.0 74,700.0
Compression (N/m) 650,000.0 1,825,000.0 405,150.0
Lateral bending (N/ ) 1.6 4.57 0.92
Flexion (N/ ) 1.4 3.88 0.87
Axial rotation (N/ ) 6.9 9.82 0.85
GM: Gardner-Morse and Stokes (2004), H: Huynh et al. (2010), M: Monteiro (2009). Please note () that Monteiro (2009) indicates the rotational
stiffness in (Nm/rad). However, we think that this is a typographical error in the respective article and should be corrected to (Nm/deg)

According to Bogduk (2005), lumbar back muscles are fascicles of the ilicostalis lumborum pars lumborum were
such muscles that exert an action on the lumbar spine and lie included on each side of the spine model. Here, we adopted
behind the plane of transverse processes, i.e. interspinales, the description of Bogduk et al. (1992), Macintosh and Bog-
intertransversarii mediales, multifidus, and lumbar erector duk (1987, 1991).
spinae (lumbar and thoracic part). Our spine model features The psoas major arises from the anterolateral aspect of
these lumbar back muscles except for the thoracic part of the the lumbar spine, i.e. from the lumbar vertebral bodies, their
lumbar erector spinae and the interspinales. Additionally, the transverse processes and the IVDs in between. Distally, its
rectus abdominis, the psoas major as well as the internal and fascicles have a common tendon that passes over the ilium
external obliques were implemented as abdominal muscles. and inserts at the lesser trochanter of the femur. Hence, it was
The transversus muscle was not included as it is the smallest attached to the vertebral bodies, to the transverse processes,
of the abdominal muscles without an anterior attachment to and to the iliopubic eminence (pelvis), following the descrip-
the skeleton and because it has a very curved line of action tion of Stokes and Gardner-Morse (1999).
(Stokes and Gardner-Morse 1999). Redirection of muscle The rectus abdominis is a medial strap-like muscle extend-
lines of action has not been implemented in demoa so far. ing caudocranially from the pubis to the sternum. Two fas-
A more detailed description including attachment points cicles were included according to the description of Bogduk
of included muscle fibres is given in Appendices 5 and 6. et al. (1992), Stokes and Gardner-Morse (1999), and Wilken-
The intertransversarii mediales is a short intersegmental feld et al. (2006).
muscle connecting adjacent lumbar vertebrae. Attachment The external oblique is the most superficial muscle of the
points of the four lumbar muscle pairs for the intertransver- lateral abdominal wall with the internal oblique lying beneath
sarii mediales were identified according to Bogduk (2005). it. Six fascicles each, running anteriorly and downward in the
Again, proposed anatomical landmarks were identified on external oblique and anteriorly and upward in the internal
the fitted graphic primitives. oblique, were included based on the descriptions of Stokes
The multifidus is the largest and most medial muscle that and Gardner-Morse (1999).
spans the lumbosacral junction. It consists of multiple fas- Muscles were modelled as Hill-type MTCs in the pre-
cicles radiating from the lumbar spinous processes and lam- sented model. See Appendix 5 for a short description and
inae. 25 fascicles in three layers arising from each lumbar Gnther et al. (2007), Haeufle et al. (2014), Mrl et al. (2012)
vertebra were implemented in the model on each side accord- for a detailed description of the muscle model.
ing to Bogduk et al. (1992), Macintosh and Bogduk (1986), Input parameters for each MTC model structure are max-
Macintosh et al. (1986). imum isometric force of the contractile element (CE) Fmax ,
The lumbar erector spinae is positioned lateral to the multi- optimal fibre length lCE,opt , and rest length of the serial elas-
fidus. Two muscles, i.e. the longissimus thoracis and the ilio- tic element lSEE,0 . All other input parameter values can be
costalis lumborum, compose the erector spinae in the lumbar set to generic values in a first approximation as in Mrl et al.
region. Each muscle has a lumbar part (longissimus thoracis (2012), which mainly refers to Gnther et al. (2007). The
pars lumborum, ilicostalis lumborum pars lumborum) and a MTC-specific values, Fmax , and the ratio of the muscle fibre
thoracic part (longissimus thoracis pars thoracis, ilicostalis length to the MTC length in an upright position of the lum-
lumborum pars thoracis) (Bogduk 2005). While the fascicles bar spine m ratio = lCE,opt /lMTC,upright were adopted from the
of the lumbar part arise from lumbar vertebrae, the fascicles literature (Christophy et al. 2011; Daggfeldt and Thorstens-
of the thoracic part arise from thoracic vertebrae and the ribs. son 2003; Delp et al. 2001; Macintosh and Bogduk 1987;
Hence, the latter were not included in the model. Five fas- Rosatelli et al. 2008). Muscle fibre length in upright position
cicles of the longissimus thoracis pars lumborum and four was set to lCE,upright = m ratio lMTC,upright , with lMTC,upright

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T. K. Rupp et al.

adapted from the spine models geometry in upright position.


For all muscles, it was assumed that lCE,upright = lCE,opt and
lSEE,0 = lMTC,upright lCE,upright . All muscle parameters are
depicted in Table 6 (Appendix 6).

2.5 Lower extremity model

The lower extremity model consists of two feet, two shanks,


two thighs, and the pelvis. It was connected to the spine model
with a free joint and IVD or bushing element between pelvis
and L5. All other joints in the lower extremity model, i.e.
talocrural, knee, and hip joint, were modelled as hinge joints.
Human stance control was implemented as if the model was
only two-dimensional in the sagittal plane. Three contact
points at each foot together with a biomechanical contact
model represented ground contact, cf. Gnther and Ruder
(2003). All in all, 70 MTCs were included in the lower
extremities. Stance control was based on the -model ver-
sion of the equilibrium point theory published by Feldman
and Levin (2009) and Feldman (1986) and restricted to the
muscles in the lower extremity. For implementation details,
please refer to Gnther and Ruder (2003), Kistemaker et al.
(2007).

2.6 Simulation

We present a new, nonlinear lumbar spine model with all


above-described spine model structures included (vertebral
bodies, ligaments, MTCs, IVDs). Additionally, we used a
state-of-the-art linear bushing element as an IVD model
variation to compare with our nonlinear IVD model (see
Sect. 2.3). Simulations of simple flexion movements in the
sagittal plane were performed with both models. The spine
model is only driven by the stimulation input STIM of the
muscles. Stimulation input for the muscles was preset to
STIMabdominal = 0.2 for the abdominal and STIMback =
0.05 for the back muscles. Remember that stimulation input
for the lower extremity muscles (STIMlowext ) was calculated
using the -control model and a very simple approach for
human stance control (Gnther et al. 2012) (see Appendix 5
(Eq. 71 ) and 2.5).
The simulation was started from an initial, upright
stance position (see 2.1) with both feet just about to touch
the ground. From there, the model settled into a quasi-
equilibrium state, which represents our initial condition. This
state was assumed to be reached when the vertical con-
tact
6 forces (three contacts in each foot) had leveled off at
i=1 Fcontact,i [0.95 m ges , 1.05 m ges ] for at least
Fig. 1 Muscle groups implemented in the spine model for the (A) 1 ms of simulation time. The model state at settling time
abdominal muscles (psoas major, rectus abdominis, internal and exter- t = tSET = tsim,start was still a neutral, upright stance posi-
nal oblique muscle), (B) multifidus, and (C) lumbar erector spinae.
Graphic primitives from CT data (Anatomium (TM), 21st Century Solu- tion. The muscle-mechanical state at t = tSET was used as an
tions Ltd/Gibraltar) were used to represent the modelled body segments initial condition for all simulations analysed in the follow-

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A forward dynamics simulation of human lumbar spine flexion

ing. Furthermore, the ligaments rest lengths were adjusted A 15


to this settled state (see Appendix 2).
The end of each simulation (t = tsim,end ) is defined as

lumbar lordosis angle L []


10
the time when the heels start lifting off the ground after the L=17.68
subject has performed a flexion movement. This is when the
vertical components of the contact forces are zero for a short 5
instance of time (Fcontact,heel = 0 N at t = tsim,end ).

0
3 Results

Our full human model was used for simulating a flexion 5


movement of the spine during upright stance. The simulated 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7

movement started in a neutral upright position and ended in t sim [s]


a flexed position (see Sect. 2.6). Spinal and abdominal mus- B 45
cles were stimulated with a constant submaximal stimula-
tion, whereas muscles in both legs were dynamically acti- 40

sagittal flexion angle S []


vated to perform stance control. As simulation results, lum- S =27.00
35
bar kinematics and loads of different biological structures are
presented (see Sect. 3.1). A model comparison between our 30
nonlinear IVD model versus a classical, linear IVD model
quantifies the differences between the two approaches on the 25
human lumbar spine level (see Sect. 3.2).
20
The overall flexion movement is represented by the lum-
bar lordosis (Polly et al. 1996) and the sagittal flexion angles 15
(Gracovetsky et al. 1995) (L , S ). The lumbar lordosis
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
angle was calculated as the difference in global orientation
t sim [s]
angles (in the sagittal plane) of IVD L5/S1 and IVD T12/L1.
Global orientation of each IVD was calculated as the mid- Fig. 2 A Lumbar lordosis angle according to Polly et al. (1996) and
angle between inferior endplate of the respective top vertebra B sagittal flexion angle according to Gracovetsky et al. (1995) as a
and superior endplate of the respective bottom vertebra. The function of the simulation time tsim starting at tSET (tsim = 0 at
tSET , tSET = 0.24 s). Overall simulation time is tsim = 0.62 s, i.e.
sagittal flexion angle is the angle between the global lon-
tsim,start = tSET = 0.24 s, tsim,end = 0.86 s
gitudinal axis (z-axis, normal to the ground) and a straight
line through the centre of S1 and C7 in the sagittal plane
(Gracovetsky et al. 1995). Both angles are depicted in Fig. 2
(see also Fig. 11 in Appendix 7). These numbers are
as a function of the simulation time tsim , i.e. tsim = 0
segmental displacements along the local longitudinal axis
at tSET , tsim,start = tSET = 0.24s, tsim,end = 0.86s and
(z: caudocranial direction) of the subjacent body relative to
tsim = 0.62s. During flexion, the torso is leaning forward
the displacement after settling (rz (t = tSET ) = 0.0 mm).
by S-nl = 27.00 , while the lumbar lordosis increases by
The local rotation angles in all lumbar interspaces increase
L-nl = 17.68 .
from L1/2 to L4/5: y 2.6 . . . 4.6 (see also Fig. 11
In all following figures, the presented results are plotted
in Appendix 7). These values are rotation angles in the
against the negative relative lordosis angle (L ) instead
local sagittal plane of the subjacent body (its local xz-
against simulation time (tsim ). L is the change in angle
plane), i.e. angular displacements between two adjacent ver-
with respect to the initial lordosis angle at time tSET . Joint
tebrae. They are likewise presented relative to rotation at tSET
kinematics and loads are depicted with reference to the local
(y (t = tSET ) = 0 ).
coordinate system of each subjacent body (centre of mass
During the simulated flexion movement, IVD forces along
of the caudal vertebra). In the following, results of the inter-
the local longitudinal axes show an increase from L1/2 to
vertebral joints L4/5 are highlighted in figures by using bold
L4/5: Fz 313N . . . 638 N. IVD moments in the local
lines.
sagittal plane (around y-axis) increase with bending forward
3.1 Simulation results and model prediction from L1/2 to L4/5: My 4.1 Nm . . . 7.5 Nm. IVD forces
and moments are depicted in Fig. 3. Restoring forces in all
The vertical displacements of the segments at t = tsim,end posterior ligaments (PLL, LF, SSL, ISL, see 2.2) during flex-
increase from L1/2 to L4/5: rz 0.34 mm . . .0.62 mm ion increase from L1/2 to L4/5 while forces of the anterior

123
T. K. Rupp et al.

A 1700
L4/5
A 700
L4/5
1600 L3/4
L3/4
L2/3
restoring force in IVD Fz [N]

600 L2/3

ligament force [N] posterior


1500 L1/2
L1/2

1400 500

1300
400
1200
300
1100

1000 200

900
0 2 4 6 8 10 12 14 16 18 100
0 2 4 6 8 10 12 14 16 18
L[ ]
L[ ]

B 18
L4/5 B 4
L4/5
restoring moment in IVD M y [Nm]

L3/4
16 3.5 L3/4
L2/3

ligament force [N] anterior


L1/2 L2/3
14 3 L1/2

12 2.5

10 2

1.5
8
1
6
0.5
4
0 2 4 6 8 10 12 14 16 18 0
L[ ] 0 2 4 6 8 10 12 14 16 18
L[ ]
Fig. 3 A IVD force components along the local longitudinal axis (z:
caudocranial direction) of the subjacent body and B IVD moments in Fig. 4 Summed total forces Ftot in A posterior and B anterior spinal
the local sagittal plane of the subjacent body (its local xz-plane) as a ligaments as a function of the negative lumbar lordosis angle, with
function of the negative lumbar lordosis angle. Bold lines are used to Ftot = Fel + Fdamp . Bold lines are used to emphasise summed total
emphasise joint forces and moments in L4/5 forces in ligaments surrounding L4/5

ligament (ALL) decrease from L1/2 to L4/5. The cumulated smallest range is depicted for the linear model with stiffness
ligament forces are depicted in Fig. 4. Selected muscle forces parameters according to Monteiro (2009) for both angles,
are depicted in Fig. 5 as forces of the muscletendon com- while the nonlinear and the linear Huynh model present sim-
plexes (FM ) normalised with respect to their respective max- ilar ranges. Larger ranges for both angles are found when
imum isometric force of the contractile element (Fmax ). All using the stiffness parameters proposed by Gardner-Morse
generated muscle forces show values of FM /Fmax < 37.4 %. and Stokes (2004) (see Table 3). Both angles are depicted
Loads are distributed homogeneously between structures. in Fig. 6 as a function of the simulation time tsim , i.e.
tsim = 0 at tSET . The overall simulation time shows lit-
3.2 Model comparison: nonlinear versus linear IVD model tle variations while start and end of each simulation do vary
(see Table 4). Hence, all models result in different lumbar and
Selected results for all linear model variations (GM: Gardner- sagittal movement in a similar period of simulation time.
Morse and Stokes (2004), H: Huynh et al. (2010), M: Mon- During the simulated flexion movement, IVD forces along
teiro (2009), for stiffness parameters, see Table 2) are pre- the local longitudinal axes show an increase in all lumbar
sented and compared to our nonlinear model. They are indi- joints in all model versions. IVD forces are similar in the
cated with nl for the nonlinear (new IVD element) and nonlinear and Huynh model at the start of simulation. Lin-
l_GM , l_H , and l_M for the three linear (bushing element) ear models using stiffness parameters by Gardner-Morse and
MB model versions, respectively. Stokes (2004) or Monteiro (2009) present higher restoring
All model versions show different settling behaviours forces at tsim,start . The Monteiro model shows less overall
with, respectively, different lumbar lordosis and sagittal flex- increase, while all other models predict a greater increase
ion angles (L , S ). The ranges differ for both angles. The in restoring forces, i. e. Fz-nl 313N . . . 638 N ver-

123
A forward dynamics simulation of human lumbar spine flexion

A 20
RA
A 25
nl
EO 20 lGM
F M /Fmax (sum of fascicles) [%]

lumbar lordosis angle L [ ]


18 IO lH
PM 15 lM

16
10

14 5

0
12
5

10 10

8 15
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
0 2 4 6 8 10 12 14 16 18
L[ ] t sim [s]

B 40 B 60
nl
MF
IT_m 55 lGM
35
F M /Fmax (sum of fascicles) [%]

sagittal flexion angle S [ ]


LTpL lH
50
IL lM
30 45

25 40
35
20
30
15
25
10 20

5 15
10
0 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
0 2 4 6 8 10 12 14 16 18
t sim [s]
L[ ]
Fig. 6 A Lumbar lordosis angle according to Polly et al. (1996) and
Fig. 5 FM /Fmax for A each abdominal muscle (grouped fascicles, RA B sagittal flexion angle according to Gracovetsky et al. (1995) as a
rectus abdominis, EO external oblique, IO internal oblique, PM psoas function of the simulation time tsim starting at tSET (tsim = 0 at tSET ,
major) and for B each back muscle (grouped fascicles, MF multifidus, tSET-nl = tSET-l_H = 0.24s, tSET-l_GM = 0.17s, tSET-l_M = 0.31s). All
IT_m intertransversarii mediales, LTpL longissimus thoracis pars lum- model versionsnonlinear (nl, solid line) versus linear (l, dotted and/or
borum, IL iliocostalis lumborum pars lumborum) as a function of the dashed lines)are depicted. The ranges differ for both angles. The
negative lumbar lordosis angle widest range is accomplished in the linear GardnerMorse model for
both angles. The linear Huynh model and the nonlinear model present
Table 3 Ranges of lumbar lordosis and sagittal flexion angles for the a mid-range, while using Monteiro data results in small ranges. Overall
nonlinear (nl) and linear IVD models simulation time is approximately the same in all models
Lumbar lordosis angle Sagittal flexion angle
Table 4 Overall simulation time as well as start and end of simulation
L-nl 17.68 S-nl 27.00 for the nonlinear (nl) and linear IVD models
Ll_GM 26.86 Sl_GM 38.80
Overall simulation time Start and end of simulation
Ll_H 19.03 Sl_H 28.48
Ll_M 6.94 Sl_M 12.90 tsim-nl 0.62s tsim,start-nl 0.24s tsim,end-nl 0.86s
GM: Gardner-Morse and Stokes (2004), H: Huynh et al. (2010), M: tsiml_GM 0.67s tsim,start-l_GM 0.17s tsim,end-l_GM 0.84s
Monteiro (2009) tsim-l_H 0.68s tsim,start-l_H 0.24s tsim,end-l_H 0.92s
tsim-l_H 0.64s tsim,start-l_M 0.31s tsim,end-l_M 0.95s
sus Fz-l_GM 254 N . . . 634 N versus Fz-l_H 260 N GM: Gardner-Morse and Stokes (2004), H: Huynh et al. (2010), M:
. . . 622 N versus Fz-l_M 150 N . . . 241 N. Respective Monteiro (2009)
IVD forces are depicted in Fig. 7.

understanding of spinal degeneration processes. The unavail-


4 Discussion ability of internal load figures in other methods highlights
the importance of the forward dynamics approach as the
Determining the internal dynamics of the human spines bio- most powerful approach to examine the mechanical cause of
logical structures is an essential step that allows enhanced biological degeneration of spinal structures. Therefore, our

123
T. K. Rupp et al.

1700 is overcome. Nevertheless, the lack of realistic muscle paths


nl
restoring force in IVD L4/5 Fz [N]

1600 lGM leads to missing transversal forces on the spinal segments


lH
lM
towards each local rotation centre. Moreover, recent litera-
1500
ture found reduced maximal muscle forces in the event of
1400 transversal loading (Siebert et al. 2014a). In future research,
1300 this model has to be improved by muscles using realistic mus-
cle paths and calculating the influence of transversal forces
1200
on the spine and on the longitudinal muscle forces itself.
1100 So far, scalability and subject-derived parameters of the
1000
developed full human body model have been achieved using
calcman for selected anthropometrical data of the spine. This
900
0 2 4 6 8 10 12 14 16 18 includes scaling of position and orientation data as well as
L[ ] partly mass distribution in the human spine. In future work, to
enhance the models subject-derived parameters, the devel-
Fig. 7 IVD L4/5 forces along the local longitudinal axis (z: caudocra- oped scaling algorithms need to include scaling of verte-
nial direction) of the subjacent body as a function of the negative lumbar
lordosis angle. All model versionsnonlinear (nl, solid line) versus lin- bral dimension, thereby mass scaling should be improved by
ear (l, dotted and/or dashed lines)are depicted including viscera and surrounding tissue mass, separately.
Additionally, scalability of insertion and origin points of lig-
aments and muscles need to be included in calcman. In a
goal was to develop a forward dynamics multi-body model following step, the algorithm needs to include a distinction
of the human body, including a detailed model of the lum- between male and female anthropometrical setup. As another
bar spine. The muscles of the legs, back, and abdomen and advanced feature to be included in the future, ageing could be
all spinal ligaments were included. Intervertebral discs were addressed by parameterising plasticity of spinal ligaments,
modelled using a nonlinear, enhanced modelling approach. intervertebral disc characteristics such as calcium content,
Using a detailed and separate model for each relevant bio- signal propagation times in muscles as well as bone density of
logical structure allows us to investigate the influence and vertebrae. These extensions will lead towards well-grounded
function of different structural elements. As a result, detailed subject-derived modelling and enhanced understanding of
dynamics of all modelled structures can be predicted. In con- spinal degeneration processes in general and with respect to
trast to inverse dynamic models, no kinematic data at all were individuals.
used as an input. Instead, the model is driven by synthetic
muscle stimulation STIM as input. In the presented model, 4.2 The nonlinear intervertebral disc model
STIM is set constant for all muscles in the spine region. For
the lower extremities, balanced upright stance, however, is One special, new feature of the full human model presented,
achieved by calculating STIM with a higher level motor con- here, is the nonlinear model of the intervertebral disc. Karajan
trol model, the -control model. Future studies can elaborate et al. (2013) addressed the shortcoming of the classical, linear
on different motion generation patterns of STIM in order to approach, the so-called bushing element used to model inter-
achieve different movements. Hence, the presented full-body vertebral discs by developing an enhanced nonlinear inter-
model can be used as a prediction tool for internal dynamics vertebral disc model. It was shown that the linear approach
of the spine. can only represent the mechanical response behaviour for a
limited range of translational and rotational displacements
4.1 The muscles line of action and model scalability for isolated intervertebral disc models. Simulation results of
our full human body model including the nonlinear interver-
In this study, only a simple movement was investigated: for- tebral disc model again show significant differences in the
ward bending. The total range of motion (ROM), i.e. the resultant movement compared to a full human body model
sagittal flexion angle, was 27.0 for the nonlinear interver- including standard, linear intervertebral disc models. How-
tebral disc element. This total ROM would already set the ever, even different parameterisations of the linear inter-
need for the determination of accurate muscular paths for vertebral disc model show significant differences in rota-
the long back muscles, for example, by using via-points tional displacement and intervertebral disc forces (compare
algorithms, wrapping surface algorithms, and dynamic Figs. 6, 7), albeit the determination of valid material proper-
via-points algorithms (Carman and Milburn 2005; Desailly ties of a humans intervertebral disc is not standardised. Stiff-
et al. 2010). However, our model geometrically separated the ness parameters are determined by experimental procedures
long back muscles to several shorter muscles parts (fasci- using complete functional spinal units (Huynh et al. 2010) or
cles) connecting less segments, thereby the redirection issue even the whole lumbar spine (Monteiro 2009). Huynh et al.

123
A forward dynamics simulation of human lumbar spine flexion

1000
(2010) used the lumped stiffness parameters to model the

internal loads in joint L4/5 Fz,load [N]


intervertebral disc and ligaments separately, thereby increas-
500
ing the overall stiffness. Monteiro (2009) presents a ques-
tionable process of determining the stiffness of a single inter- 0
vertebral disc from stiffness data of a whole lumbar spine.
Gardner-Morse and Stokes (2004) present measurements to 500
determine the stiffness of single lumbar intervertebral discs
including surrounding ligaments. They also present percental 1000

changes when removing all ligaments. Comparing the linear MTC


1500 IVD
GardnerMorse model and our nonlinear model, we found LIG
our model to be stiffer in total. However, restoring forces tot
2000
in the nonlinear model are in the same order of magnitude 0 2 4 6 8 10 12 14 16 18
with in vivo data, whereas restoring forces of the linear L[ ]
bushing elements according to Gardner-Morse and Stokes
Fig. 8 Internal load components in joint L4/5, i.e. forces along the lon-
(2004) undershoot these in vivo results. Still, we argue that
gitudinal axis (caudocranial) of the virtual joint coordinate system pro-
a valid comparison between nonlinear and linear interverte- duced by surrounding muscles (MTC), ligaments (LIG), and the IVDs
bral disc models is lacking and can only be accomplished (IVD) as a function of the negative lumbar lordosis angle. Additionally,
with improved nonlinear parameters. So far, the nonlinear the sum of all internal loads is depicted
intervertebral disc model is based on an idealised geometry,
its inherent inhomogeneous structure is not included, yet.
The determination of nonlinear parameters from experimen- exist due to the coordinate transformation between the two
tal measurements and the proposed homogenisation tech- reference systems: local IVD coordinate system in Fig. 3a and
nique of Karajan et al. (2013) would overcome these issues. virtual joint coordinate system in Fig. 8. In the hypothetical
It needs to be accomplished and used to model an improved case of modelling just one structure for the spinal segment,
nonlinear intervertebral disc model. Then, nonlinear and lin- e. g. the classical bushing element or an algebraic constraint,
ear intervertebral disc models can be compared in order to only one joint force would be calculated. This virtual joint
identify the additional value of using nonlinear interverte- force would be equal to the sum of the forces produced by the
bral disc models in full human body models. Additionally, surrounding biological structures, which is depicted by the
the intervertebral disc model needs to be enhanced to rep- red line (tot) in Fig. 8. In the static case, its value would be
resent the complete spinal motion segment. Therefore, facet exactly the gravitational load due to the masses cranial to L5.
joints have to be included, which play a significant role dur- The actual IVD force is 34 times higher than the virtual joint
ing flexion movement of the spine. force. Assuming the virtual joint force to represent the IVD
load would correspondingly underestimate the physiological
4.3 The load sharing of biological structures during flexion load by 34 times.
movement Considering all single structures of the same type lumped
into their net effect, the internal forces resulting from the 90
The biological joint of a spinal segment is a hypothetical MTCs dominate the internal forces carried by the 11 liga-
construct. In our model, this joint is composed of pure force ment parts crossing the L4/5 joint. Interestingly, this can be
interaction, namely the IVD, the muscles, and the ligaments. observed, although the corresponding muscle stimulations
The sum of all forces composing the joint is the net joint STIM are at a sub-maximal level, i.e. 5 % of maximal stimu-
force. We assume this force to act in a virtual joint coordinate lation for the back muscles and 20 % of maximal stimulation
system located between two adjacent vertebrae. Technically, for the abdominal muscles. The presented spine model would
in multi-body systems, such a biological joint is a 6-DOF allow to depict the individual contribution of each modelled
element connecting parent and child bodies. Thereto, a local biological element, for example, the M. longissimus thoracis
joint coordinate system must be defined on each body. We pars lumborum part crossing the L4/5 joint (LTpL_L4).
constructed a corresponding virtual joint coordinate system
by calculating the arithmetic mean for each single component 4.4 The validation of human full-body models
of adjacent local joint coordinate systems.
Internal force components along the longitudinal axis A proper validation of a musculoskeletal full-body model
(caudocranial) of the virtual joint coordinate system are of the human body is a difficult task to perform. This task
depicted for L4/5 in Fig. 8. The caudocranial force carried by requires several steps. The explanatory power of the model
the intervertebral disc in Fig. 8 is almost identical to the IVD crucially depends on the quality of the taken steps. To the
force component in Fig. 3a. Slight differences in the values best of our knowledge, not a single musculoskeletal model,

123
T. K. Rupp et al.

including ours, has yet been published that was rigorously in relaxed standing and 1,944 N in a flexed position. Our
validated against literature or specifically recorded biologi- model predicts longitudinal IVD forces of 942 N and 1,681 N,
cal data. For models, like the one presented, a consistent and respectively. We conclude that our model can already predict
comprehensive data set of a realistic geometry, exact material valid internal loads of the spinal column in standing and in
properties, unique kinematics, precisely defined (biological) flexion movements, i.e. in physiological quasi-static condi-
constraints, exact initial values (potential energy), and pre- tions.
cisely measured loads would be needed. This prediction of quasi-static conditions was made pos-
For the development of our model, we based all geometri- sible due to the modelling of realistic mechanical boundary
cal information on the most comprehensive data set available. conditions, physiological parameterisation of all modelled
To generate a generic geometry of the spine, we had to merge force-bearing structures, and realistic stimulation input lev-
several data sets (see Appendix 1). Since we have included els. Eventually, our model is intended to be used in a variety
Hill-type muscles as biological drives, we used established of biological movement tasks, including dynamic loading
model parameters (see Appendices 5, 6). The implemented conditions. Consequently, we performed a further validation
muscle model is not able to predict transversal muscle forces step. We simulated an impact situation inducing a shock wave
applied to the bodies. This muscle feature has been recently propagation through the body (see Appendix 8). As in the
addressed (Siebert et al. 2014a, b), and future model versions static condition, the model output is in good accordance with
will incorporate that. Ligaments were modelled based on sin- the literature data. It predicts realistic shock wave propa-
gle in vitro experiments (see Appendices 2, 3). All lumbar gation velocity along the spinal column and time delays of
intervertebral discs were modelled using a recently published acceleration peaks along the whole body.
approach, which is based on a FE model of the L4/5 disc
and calibrated with experimental data. So far, we have not 4.5 Application and use of the presented model
included any information on how intervertebral disc parame-
ters are scaled along the spinal column. With that in mind, The presented multi-body model can predict internal loads
the stiffness of all intervertebral discs above L4/5 should be of the spine. Moreover, it can be used as a technical tool to
overestimated, and the displacements of the discs are under- understand the biomechanical design of the human lumbar
estimated in our result. spine. The field of application is wide. The model can be used
Despite the effort of using validated isolated model parts to determine internal spinal loads for different movements,
like spine geometry, MTCs, ligaments, and intervertebral for example, by including a more complex movement con-
discs, we cannot assume the validity of the overall model trol. It can be used for surgery research, for example, a spinal
a priori. This is due to the nonlinear interplay of the model fusion can be simulated by limiting the degrees of freedom
parts. Additional experiments analysing the complete non- between two vertebrae. It can be used to test the effect of
linear system are inevitably needed in order to compare sim- intervertebral disc implants, if they are modelled as a com-
ulation with biology. Several studies found in the literature plex force element similar to our intervertebral disc model.
report on full spinal motion or local spine kinematics, cf. It can also be used to study ageing. For this, the parameter-
Hayes et al. (1989), Ibarz et al. (2013), Pearcy and Portek isation of the modelled biological structures can be varied
(1984), White and Panjabi (1990). Some studies have com- to match that of a very old person. Then, the resulting dif-
bined global spine kinematic data with local IVD force data, ferences in internal loads can be examined. Altogether, the
cf. Wilke et al. (2001, 1999). As already stated, there is forward dynamics approach as presented here may lead to
no experimental data set that resolves kinematics and loads an enhanced understanding of mechanical cause of biologi-
of force-bearing structures composing the biological joints cal degeneration or so-called natural ageing.
of the spine. Lacking comprehensive data sets, we com- Back pain is not understood, yet (Hancock et al. 2011;
pared our model output with the best data sets on local Langevin and Sherman 2007; Waddell 1987), albeit a direct
and global observables available. For a detailed compari- relationship between back pain and biological degeneration
son of our model output to the literature data, we refer to has been hypothesised (Millecamps et al. 2012), although not
Appendix 7. In summary, the comparison reveals that our been proven true so far. This study aimed at providing a con-
predicted longitudinal joint displacements in the spine and sistent, detailed, and quantitative data set of all mechanical
angular displacements of the IVDs tend to be too low, but are variables that might determine biological degeneration, with
in accordance with the tendency of the recorded amplitudes the presented model is possible to quantify forces, stresses,
to increase from L4/5 to L1/2. However, the most important strains, and rates thereof, as well as repetitive load profiles
comparison with the literature data is based on the prediction acting on structures. For example, we doubt that increased
of the longitudinal IVD forces. Wilke et al. (2001), Wilke longitudinal loads automatically result in increased proba-
et al. (1999) measured intradiscal pressure from which we bility of negative physiological effects, i.e. wear and tear.
calculated longitudinal IVD forces in L4/5 of 774 N900 N Intervertebral disc material might be more sensitive to shear

123
A forward dynamics simulation of human lumbar spine flexion

450
strain than to axial strain, with a higher risk of failure. This
model can be used as a starting point model to include pain
models in order to contribute towards pain research in the
future. 400
For all mentioned reasons, we provide the developed
multi-body model as C/C++ code as well as the sim- and ani-
binaries of our multi-body simulation package demoa under 350
the BSD License (see electronic supplementary material) to
be used by all researchers in further studies.
300
Acknowledgments The authors would like to thank the German
Research Foundation (DFG) for financial support of the project within
the Cluster of Excellence in Simulation Technology (EXC 310/1) at the

z [mm] longitudinal axis


University of Stuttgart.
T.R. and S.S. have received funding from the (European Union) Seventh 250
Framework Programme (FP7/20072013) under Grant Agreement No.
246994.

200

Appendix 1: Generated anthropometric data set:


vertebral position, orientation, and dimension
150

An average data set of vertebral positions was calculated


from the literature data (Ashton-Miller and Schultz 1997;
Belytschko 1978; El-Rich and Shirazi-Adl 2004; Kitazaki 100

and Griffin 1997) to be used by calcman. They determined


global orientation and position of vertebrae using skin mark-
ers. The vertebral position is defined as the position of the fAvg (z)
50 fAvg (z) +/
geometric centre of each vertebral body with respect to the fAshton (z)
fBelytschko (z)
global reference frame. S1 was positioned in the centre of fKitazaki (z)
the pelvis. Position data from each literature data set was 0
fRich (z)
normalised in length to one reference trunk height, i.e. each 60 45 30 15 0 15
data set was normalised to the same caudocranial distance (z- x [mm] sagittal axis
value) of T1-L5, h T1-L5,Avg = 458.1mm h T1-L5,Belytschko .
Fig. 9 Anthropometric data set functions fitted to the position data
Then, a polynomial fit was estimated for each data set (see of vertebral bodies (centre) in healthy male humans. All polyno-
Fig. 9, f Ashton , f Belytschko , f Rich and f Kitazaki ). These four fits mial fits f Ashton (z) (Ashton-Miller and Schultz 1997), f Belytschko (z)
for x = f (z) were averaged by calculating the mean coeffi- (Belytschko 1978), f Rich (z) (El-Rich and Shirazi-Adl 2004), and
cients of each polynomial. The resulting function (sixth-order f Kitazaki (z) (Kitazaki and Griffin 1997) were scaled to the reference
height of h T1-L5,Avg = 458.1 mm from T1 to L5. f Avg (z) depicts the
polynomial) writes mean data set used for scaling in calcman, the thin grey lines capture
its standard deviation f Avg (z) + / . Plus sign indicates the position
f Avg (z) = 0.015 mm+0.201z 1.12 103 mm1 z 2 of each vertebral centre L5 to T1. The origin is equal to the position
1.2105 mm2 z 3 +7.0108 mm3 z 4 point of L5. The sagittal axis from dorsal to ventral is equal to the x-
axis, while the longitudinal axis from caudal to cranial is equal to the
1.5 1010 mm4 z 5 z-axis
+1.01013 mm5 z 6 . (2)

The average position data on the longitudinal axis includ- modelled as a cylinder (see below), although real ver-
ing standard deviation and the basis data sets are presented tebrae are slightly wedge-shaped. The calculated orien-
in Fig. 9. Calcman calculates the subject-derived height tations were compared with the experimental data from
(h T1-L5 ) and, with that, scales the z-position of each vertebra the literature (Ashton-Miller and Schultz 1997; Campbell-
by the ratio h T1-L5 / h T1-L5,Avg while leaving the x-position Kyureghyan et al. 2005), which are usually presented
unscaled (Table 1). as upper endplate orientations in the sagittal plane. For
Each vertebral orientation was defined as the normal of this, we fitted graphic primitives from computed tomogra-
the curve (Eq. 2) at its position aligning with the anterior phy (CT) data (Anatomium (TM), 21st Century Solutions
posterior direction of the vertebra. Each vertebra was Ltd/Gibraltar) that represent T1 to S1, to their respective

123
T. K. Rupp et al.

cylinder primitives and estimated the upper endplate orien-


tation (Table 1). All three data sets vary locally in the range
of a few degrees, which is well represented by their standard
deviations.
Vertebral dimensions, i.e. vertebral height, depth, and
width, were determined for the entire spine, i.e. C3 to S1.
The study by Gilad and Nissan (1986) was used as a basis.
However, it only includes cervical and lumbar dimensions.
Missing data were determined by parameter scaling of data
sets from Panjabi et al. (1991, 1992), White and Panjabi
(1990). For example, depths for the whole spine included in
Panjabi et al. (1992, 1991), White and Panjabi (1990) were
scaled to the basis depths in Gilad and Nissan (1986) in order
to determine missing vertebral depths in the thoracic spine.
The cylinders height was set to the maximum of dor-
sal and ventral height (Eq. 35 ), its radius to the maximum
of depth and width (Eq. 36 ). This allows an easy inclusion
of the mass of the spinous and transverse processes. It is Fig. 10 Forcelength relation of the spinal ligament. Four independent
parameters were used such as lLIG,0 (rest length), ULIG,nll (relative
assumed that their mass approximately balances the over- stretch at nonlinearlinear transition), FLIG,0 (both force at the tran-
estimation by using the maximum height and ignoring the sition and force increase in the linear part), and ULIG,l (relative addi-
wedge shape of each vertebral body. The vertebral mass tional stretch in the linear part providing a force increase in FLIG,0 ).
(Eq. 33 ) was calculated on the basis of each cylinders vol- The transition between the initial nonlinear and the linear region is
located at lLIG,nll = (1 + ULIG,nll ), the exponent for the initial nonlin-
ume (Eq. 34 ) and the lumbar vertebrae bone density lumbar = ear relation is LIG,nll = ULIG,nll /ULIG,l . The parameters of relevant
6001,000 kg/m3 (Nigg and Herzog 2007). The moment of and included spinal ligaments are given in Table 5. They were derived
inertia tensor follows from the cylinders parameters (see from experimental data (Chazal et al. 1985)
Eqs. (3)1,2 ):
Fel,LIG (lLIG )

Icyl,xx = Icyl,yy = 1/12 m vert,i h 2vert,i + 1/4 0 lLIG < lLIG,0
m vert,i rvert,i
2
, = K LIG,nl (lLIG lLIG,0 )LIG,nll lLIG < lLIG,nll ,

FLIG,0 + K LIG,l (lLIG lLIG,nll ) lLIG lLIG,nll
Icyl,zz = 1/2 m vert,i rvert,i
2
(4)
with m vert,i = Vvert,i lumbar 3/2,
Vvert,i = rvert,i,width
2
h vert,i , where lLIG is its length. Its parameters are
h vert,i = max{h vert,i,dorsal , h vert,i,ventral }, lLIG,nll = (1 + ULIG,nll ) lLIG,0 ,
rvert,i = max{rvert,i,depth , rvert,i,width }. (3) LIG,nll = ULIG,nll /ULIG,l ,
K LIG,nl = FLIG,0 /(ULIG,nll lLIG,0 )LIG,nll ,
K LIG,l = FLIG,0 /(ULIG,l lLIG,0 ). (5)
Appendix 2: Nonlinear ligament model They were derived from four independent parameters such
as lLIG,0 (rest length of ligament), ULIG,nll (relative stretch
Various studies on ligaments confirm a nonlinear stress at nonlinearlinear transition), FLIG,0 (both force at transi-
strain characteristic for ligaments (Chazal et al. 1985; Pin- tion and force increase in linear part), and ULIG,l (relative
tar et al. 1992). For our lumbar spine model, the spinal lig- additional stretch in linear part providing the force increase
aments were modelled as nonlinear straight-line elements FLIG,0 ), cf. Fig. 10. These parameters were partly extracted
based on the experimental results by Chazal et al. (1985), from tensile experiments on 43 human spinal ligaments per-
Panjabi et al. (1982). The function describing the spinal liga- formed by Chazal et al. (1985). For five spinal ligaments, i.e.
ments stressstrain characteristics was assumed to be contin- anterior longitudinal (ALL) and posterior longitudinal lig-
uously differentiable (C 1 continuity) between an initial non- ament (PLL), ligamentum flavum (LF), supra-spinal (SSL),
linear region (up to A) and a constant stiffness at higher loads and interspinal (ISL) ligament, Chazal et al. (1985) estimated
(A-B, see Fig. 10). The concave region at even higher forces tension and elongation at transition (point A), at the end of
is not shown here. Hence, the forcelength characteristic of the linear phase (point B) and at the apex of the tension elon-
a spinal ligament is modelled as gation curve. The arithmetic means of the extracted force and

123
A forward dynamics simulation of human lumbar spine flexion

elongation data at A and B (FA , lA , FB , lB ) were used to cal- is then equally distributed by equally distributing FLIG,0
culate three input parameters of the ligament characteristic between multiple lines.
(ULIG,nll , ULIG,l , FLIG,0 ). These input parameters were A velocity-dependent damper was also included in order to
determined separately for each of the five ligaments. account for the ligaments nonlinear viscoelastic behaviour,
The ligaments rest length (lLIG,0 ) was extracted from the i.e.
models geometry. It is accepted that spinal ligaments are
not in a strain-free state when the spine is in its neutral Fdamp,LIG = Fel,LIG dLIG vLIG with
anatomical position during upright stance. Pre-strain data for dlLIG(t)
with vLIG = , dLIG = 1.0 s m1
the spinal ligaments were taken from the literature (Aspden dt
1992; Nachemson and Evans 1968; Robertson et al. 2013) and consequently Ftot,LIG = Fel,LIG (1 + dLIG vLIG ).
and used to determine the ligaments rest length in the neutral (6)
position. The neutral position was approximated by simulat-
ing an initial settling of the lumbar spine model (see 2.6, neu- According to Gerritsen et al. (1995), the damping force
tral position). In that state, each ligaments rest length was depends on the elastic force Fel,LIG and is scaled by a damp-
calculated by the distance between two ligaments attach- ing coefficient dLIG . This avoids discontinuity and numerical
ment points (lLIG,SET [m]) and the respective pre-strain ( LIG stabilities.
[ ]): lLIG,0 = lLIG,SET /(1 + LIG ).
As proposed by Panjabi et al. (1982), ligaments with pla-
nar attachment areas, like the ALL, LF, and ISL, can be Appendix 3: Ligament parameters
approximated by more than one pair of attachment points, i.e.
multiple lines for one ligament. Their characteristic (Eq. 4) See Table 5.

Table 5 Ligament modelling parameters for the nonlinear MB model providing the force increase FLIG,0 ) and (pre-strain of ligament), for
version, i.e. lLIG,0 (rest length of ligament), ULIG,nll (relative stretch at all included spinal ligaments, i.e. anterior longitudinal (ALL) and poste-
nonlinearlinear transition), FLIG,0 (both force at transition and force rior longitudinal ligament (PLL), ligamentum flavum (LF), supraspinal
increase in linear part), ULIG,l (relative additional stretch in linear part (SSL), and interspinal (ISL) ligament
Ligament Name of ligaments Non-lin/IVD
single or multiple line
lLIG,0 (m) ULIG,nll K LIG,nl (N/m2.5 )

ALL lA =1.5 mm, lB =5.0 mm, FA = 55 N, FB = 456 N, = 6.8 %


LIG,nll = 3.203, K LIG,l =3.9104 N/m
Ligament_S1_L5_ALL_lig1 0.013036 0.116600 1.95 1010
Ligament_L5_L4_ALL_lig1 0.008311 0.182894 1.95 1010
Ligament_L4_L3_ALL_lig1 0.008846 0.171823 1.95 1010
Ligament_L3_L2_ALL_lig1 0.009805 0.155019 1.95 1010
Ligament_L2_L1_ALL_lig1 0.008630 0.176131 1.95 1010
Ligament_S1_L5_ALL_lig2 0.012268 0.123897 1.95 1010
Ligament_L5_L4_ALL_lig2 0.007993 0.190175 1.95 1010
Ligament_L4_L3_ALL_lig2 0.008999 0.168900 1.95 1010
Ligament_L3_L2_ALL_lig2 0.009793 0.155217 1.95 1010
Ligament_L2_L1_ALL_lig2 0.008952 0.169803 1.95 1010
Ligament_S1_L5_ALL_lig3 0.013036 0.116600 1.95 1010
Ligament_L5_L4_ALL_lig3 0.008311 0.182894 1.95 1010
Ligament_L4_L3_ALL_lig3 0.008846 0.171823 1.95 1010
Ligament_L3_L2_ALL_lig3 0.009805 0.155019 1.95 1010
Ligament_L2_L1_ALL_lig3 0.008630 0.176131 1.95 1010

123
T. K. Rupp et al.

Table 5 continued
Ligament Name of ligaments Non-lin/IVD
single or multiple line
lLIG,0 (m) ULIG,nll K LIG,nl (N/m2.5 )

PLL lA = 0.9 mm, lB = 3.2 mm, FA = 48.33 N, FB = 342.5 N, = 13.0 %


LIG,nll = 2.409, K LIG,l = 12.7 104 N/m
Ligament_S1_L5_PLL_lig 0.044567 0.020569 1.00 109
Ligament_L5_L4_PLL_lig 0.008537 0.107381 1.00 109
Ligament_L4_L3_PLL_lig 0.007142 0.128359 1.00 109
Ligament_L3_L2_PLL_lig 0.009610 0.095393 1.00 109
Ligament_L2_L1_PLL_lig 0.010251 0.089428 1.00 109
LF lA = 1.6 mm, lB = 3.8 mm, FA = 75 N, FB = 315 N, = 10.0 %
LIG,nll = 2.327, K LIG,l = 3.6 104 N/m
Ligament_S1_L5_LF_lig1 0.023005 0.069549 8.03 107
Ligament_L5_L4_LF_lig1 0.017324 0.092355 8.03 107
Ligament_L4_L3_LF_lig1 0.020142 0.079437 8.03 107
Ligament_L3_L2_LF_lig1 0.021107 0.075805 8.03 107
Ligament_L2_L1_LF_lig1 0.023853 0.067077 8.03 107
Ligament_S1_L5_LF_lig2 0.025083 0.063789 8.03 107
Ligament_L5_L4_LF_lig2 0.017671 0.090542 8.03 107
Ligament_L4_L3_LF_lig2 0.020141 0.079441 8.03 107
Ligament_L3_L2_LF_lig2 0.021098 0.075835 8.03 107
Ligament_L2_L1_LF_lig2 0.023958 0.066783 8.03 107
Ligament_S1_L5_LF_lig3 0.023005 0.069549 8.03 107
Ligament_L5_L4_LF_lig3 0.017324 0.092355 8.03 107
Ligament_L4_L3_LF_lig3 0.020142 0.079437 8.03 107
Ligament_L3_L2_LF_lig3 0.021107 0.075805 8.03 107
Ligament_L2_L1_LF_lig3 0.023853 0.067077 8.03 107
ISL lA = 1.5 mm, lB = 3.8 mm, FA = 40.14 N, FB = 215 N, = 4.6 %
LIG,nll = 2.960, K LIG,l = 2.6 104 N/m
Ligament_S1_L5_ISL_lig1 0.023083 0.066846 2.81 109
Ligament_L5_L4_ISL_lig1 0.012625 0.122221 2.81 109
Ligament_L4_L3_ISL_lig1 0.016457 0.093759 2.81 109
Ligament_L3_L2_ISL_lig1 0.018955 0.081402 2.81 109
Ligament_L2_L1_ISL_lig1 0.025347 0.060875 2.81 109
Ligament_S1_L5_ISL_lig2 0.023501 0.065657 2.81 109
Ligament_L5_L4_ISL_lig2 0.011996 0.128628 2.81 109
Ligament_L4_L3_ISL_lig2 0.014388 0.107241 2.81 109
Ligament_L3_L2_ISL_lig2 0.018647 0.082747 2.81 109
Ligament_L2_L1_ISL_lig2 0.025289 0.061014 2.81 109
Ligament_S1_L5_ISL_lig3 0.022529 0.068489 2.81 109
Ligament_L5_L4_ISL_lig3 0.011197 0.137807 2.81 109
Ligament_L4_L3_ISL_lig3 0.013926 0.110797 2.81 109
Ligament_L3_L2_ISL_lig3 0.018295 0.084339 2.81 109
Ligament_L2_L1_ISL_lig3 0.026143 0.059021 2.81 109

123
A forward dynamics simulation of human lumbar spine flexion

Table 5 continued
Ligament Name of ligaments Non-lin/IVD
single or multiple line
lLIG,0 (m) ULIG,nll K LIG,nl (N/m2.5 )

SSL lA = 1.5 mm, lB = 3.8 mm, FA = 40.14 N, FB = 215 N, = 12.0 %


LIG,nll = 2.960, K LIG,l = 7.7 104 N/m
Ligament_S4_S3_SSL_lig 0.029616 0.052100 8.42 109
Ligament_S3_S2_SSL_lig 0.036568 0.042195 8.42 109
Ligament_S2_S1_SSL_lig 0.034092 0.045260 8.42 109
Ligament_S1_L5_SSL_lig 0.039796 0.038773 8.42 109
Ligament_L5_L4_SSL_lig 0.039338 0.039224 8.42 109
Ligament_L4_L3_SSL_lig 0.034178 0.045146 8.42 109
Ligament_L3_L2_SSL_lig 0.037396 0.041261 8.42 109
Ligament_L2_L1_SSL_lig 0.054495 0.028314 8.42 109
Pre-strain data for all relevant spinal ligaments were taken from the literature (Aspden 1992; Nachemson and Evans 1968; Robertson et al. 2013).
The remaining four parameters were derived using experimental data from tensile tests (Chazal et al. 1985). Here, force and elongation at transition
(FA , lA ) and at the end of the linear phase (FB , lB ) were used

Appendix 4: Development of specific IVD model a reaction force and moment due to an applied deformation
state (combination of displacement and rotation). A parame-
In MB models, IVDs are either modelled as one force ele- terisation using a cubic polynomial turned out to deliver the
ment or one force element is used to capture the mechanical best fit of the resulting forces and moments gathered at the
response of the IVD as well as its surrounding ligaments and varying deformation states, i. e. sampling points, which can
muscles, i.e. lumped modelling approach for one functional be related to the displacements and rotations of the MB sys-
spinal unit. The mechanical response of an IVD (Huynh et al. tem defined in demoa. For more detailed information on the
2010) or a functional spinal unit (Christophy et al. 2011; representation, the reader is referred to Karajan et al. (2013).
Monteiro 2009) is usually modelled using a linear and decou-
pled bushing element (6-DOF spring-dashpot element) as a
connecting force element. Stiffness and damping parameters Appendix 5: Hill-type muscles in MB models
are taken from experimental measurements (Ashton-Miller
and Schultz 1997; Berkson et al. 1979; Eberlein et al. 2004; In forward dynamics MB models, muscles are often mod-
Gardner-Morse and Stokes 2004; Hirsch and Nachemson elled as Hill-type MTCs (Haeufle et al. 2014). This labelling
1954; Schultz et al. 1979; Virgin 1951). Experimental data refers to A.V. Hillss experimental finding (Hill 1938) that
clearly demonstrate the nonlinear nature of these biological the forcevelocity relation of a muscles fibre is a hyper-
tissues. Hence, it is linearised to be used as model parame- bola. Thus, Hill-type models are phenomenologically based
ters for the linear elements in other MB models (Huynh et al. macroscopic lumped parameter models. Such a model usu-
2010; Monteiro 2009). So far, model parameters differ, as ally consists of a contractile element (CE), a serial, and a par-
experimental results cover a wider range. allel elastic element. The corresponding contraction (Eq. 71 ,
Instead, a recently developed IVD model was used in our CE length lCE ), and activation dynamics (Eq. 72 , activity q
MB model and implemented in demoa. It captures the nonlin- with 0 q 1) of a muscle are described by first-order
ear and coupled mechanical response of IVDs in the lumbar differential equations:
region from pelvis to vertebra L1 (Karajan et al. 2013). In
particular, a FE model of the IVD (Karajan 2012) was used to lCE = fl (lCE , lMTC , q),
pre-compute the mechanical behaviour of the IVD in terms of q = f q (q, STIM) (7)
stresses and strains. The FE model of the IVD is based on the
theory of porous media. It is capable of capturing the porous with lMTC : length of MTC, STIM stimulation input. STIM
microstructure of the IVD. The mechanical response of the is calculated by our simple lambda-control model, a bio-
IVD due to several applied deformation states was captured at inspired motor control model. It represents the electrical
its centre of gravity by homogenisation via an integration of stimulation signal (summed transmembrane potential) on the
the resulting stresses at the connecting surface of the adjacent muscles surface and can be compared with surface elec-
vertebra. Thus, each of the homogenised results represents tromyography (sEMG). Gnther et al. (2007) included an

123
T. K. Rupp et al.

additional damping component parallel to the serial elastic for a detailed description of the muscle model. It was imple-
element. Hence, the right-hand side of Eq. (7)1 also depends mented in demoa and used for all MTCs in the presented full
on lMTC . By using this modified Hill-type muscle model, human MB model.
movement control is expected to be more feasible, because
eigenoscillations are damped due to the interaction of muscle Appendix 6: Muscle parameters
and segment inertia (Gnther et al. 2007). We refer to Gn-
ther et al. (2007), Haeufle et al. (2014), Mrl et al. (2012) See Table 6.

Table 6 Muscle modelling parameters: maximum isometric force of the contractile element Fmax , optimal fibre length lCE,opt , and serial elastic
element lSEE,0
Muscle Name of fascicle Fmax (N) m ratio lSEE,0 (m) lCE,opt (m)

Multifidus [C] [R]


Laminar fibres MF_m1.laminar 9.00 0.681 0.017954 0.038329
MF_m2.laminar 10.00 0.681 0.015977 0.034108
MF_m3.laminar 11.00 0.681 0.016264 0.034721
MF_m4.laminar 8.00 0.681 0.017277 0.036884
MF_m5.laminar 17.00 0.681 0.013536 0.028897
Single fascicles MF_m1s 18.00 0.661 0.028638 0.055839
MF_m2s 18.00 0.677 0.024826 0.052035
MF_m3s 25.00 0.661 0.028090 0.054771
MF_m4s 21.00 0.562 0.032217 0.041338
MF_m5s 10.00 0.562 0.018348 0.023542
Multi fascicles MF_m1t.1 19.00 0.730 0.030473 0.082389
MF_m1t.2 17.00 0.730 0.039516 0.106839
MF_m1t.3 28.00 0.730 0.049693 0.134355
MF_m2t.1 18.00 0.727 0.029825 0.079423
MF_m2t.2 23.00 0.727 0.040548 0.107979
MF_m2t.3 23.00 0.727 0.042400 0.112911
MF_m3t.1 24.00 0.709 0.049223 0.119927
MF_m3t.2 24.00 0.709 0.047770 0.116389
MF_m3t.3 24.00 0.709 0.046875 0.114207
MF_m4t.1 21.00 0.667 0.028528 0.057141
MF_m4t.2 21.00 0.667 0.039598 0.079316
MF_m4t.3 21.00 0.667 0.051079 0.102311
MF_m5t.1 10.00 0.667 0.042376 0.084879
MF_m5t.2 10.00 0.667 0.029770 0.059629
MF_m5t.3 10.00 0.667 0.017582 0.035218
Erector spinae [C] [C], [De], [M]
Iliocostalis lumborum pars lumborum IL_L1 50.00 0.274 0.136660 0.051577
IL_L2 71.00 0.274 0.111749 0.042175
IL_L3 84.00 0.274 0.088155 0.033271
IL_L4 87.00 0.274 0.061923 0.023370
Longissimus thoracis pars lumborum LTpL_L1 36.00 0.419 0.108408 0.078180
LTpL_L2 42.00 0.433 0.088451 0.067547
LTpL_L3 47.00 0.436 0.069353 0.053613
LTpL_L4 51.00 0.438 0.051840 0.040402
LTpL_L5 53.00 1.000 0.000002 0.065870

123
A forward dynamics simulation of human lumbar spine flexion

Table 6 continued
Muscle Name of Fascicle Fmax (N) m ratio lSEE,0 (m) lCE,opt (m)

Intertransversarii mediales [Da] est.


IT_m1 42.84 0.500 0.013848 0.013848
IT_m2 42.84 0.500 0.014834 0.014834
IT_m3 42.84 0.500 0.011768 0.011768
IT_m4 42.84 0.500 0.011933 0.011933
Rectus Abdominis [C] [De]
RA 261.00 0.788 0.076703 0.285103
External Oblique [C] [C]
EO1 90.00 0.389 0.068556 0.043647
EO2 107.00 0.410 0.070880 0.049256
EO3 112.00 0.455 0.061347 0.051216
EO4 108.00 0.470 0.063216 0.056060
EO5 126.00 0.480 0.057528 0.053103
EO6 183.00 0.500 0.046370 0.046370
Internal Oblique [C] [C]
IO1 85.00 0.400 0.077525 0.051683
IO2 103.00 0.400 0.081398 0.054265
IO3 104.00 0.400 0.102389 0.068259
IO4 123.00 0.600 0.072381 0.108572
IO5 108.00 0.600 0.055813 0.083719
IO6 95.00 0.600 0.050050 0.075075
Psoas [C] [C]
Ps_L1_VB 97.00 0.800 0.054573 0.218293
Ps_L1_TP 28.00 0.800 0.054338 0.217352
Ps_L2_TP 97.00 0.800 0.048180 0.192718
Ps_L3_TP 46.00 0.800 0.041697 0.166789
Ps_L4_TP 74.00 0.800 0.036397 0.145589
Ps_L5_TP 80.00 0.800 0.031366 0.125463
Ps_L5_VB 88.00 0.800 0.027617 0.110468
Ps_L1_L2_IVD 55.00 0.800 0.051320 0.205279
Ps_L2_L3_IVD 55.00 0.800 0.044123 0.176491
Ps_L3_L4_IVD 17.00 0.800 0.037173 0.148691
Ps_L4_L5_IVD 36.00 0.800 0.030597 0.122387
All other input parameter values can be set to generic values in a first approximation as in Mrl et al. (2012), which mainly refers to Gnther
et al. (2007). Fmax and the ratio of the muscle fibre length to the MTC length m ratio = lCE /lMTC were adopted from the literature and thus
lCE,0 = m ratio lMTC,init . In turn, lMTC,init was adapted from the spine models geometry in the first time step of the simulation. For all muscles, it
was assumed that lCE,0 = lCE,opt and lSEE,0 = lMTC,init lCE,0 . The source of data is given at the top of each column: [C] Christophy et al. (2011),
[Da] Daggfeldt and Thorstensson (2003), [De] Delp et al. (2001), [M] Macintosh and Bogduk (1987), [R] Rosatelli et al. (2008). est. indicates that
these data were not given explicitly, but were estimated graphically

Appendix 7: Comparison with the literature data used for comparison. In the following, vertical transla-
tional and angular displacements, and IVD forces of the
Kinematic data from the literature cannot be compared presented lumbar spine model are compared with the lit-
directly with results from experimental studies because erature data. Additionally, the resultant IVD forces of the
investigated overall movements differ. Some studies present nonlinear intervertebral disc model included into the spine
flexionextension results in a combined way, others present model are compared with results of three lumbar spine
data, measured with less or more flexion amplitudes. There- model variations including the classical, linear interverte-
fore, relative changes and the order of magnitude were bral disc model for three different parameter sets. The resul-

123
T. K. Rupp et al.

A 0 3
our simulation
Hayes et al. (1989)
L4/5
vert. displacement in IVD r z [103 m]
Li et al. (2009)

range of vert. displacement in IVD [mm]


L3/4
0.1 L2/3 2.5
L1/2
0.2
2

0.3
1.5

0.4
1
0.5
0.5
0.6
0 2 4 6 8 10 12 14 16 18
0
L[ ] L1/2 L2/3 L3/4 L4/5

B 5 Fig. 12 Vertical displacements in the lumbar joints, w.r.t local joint


L4/5 coordinate system, increase from cranial to caudal. In vitro studies
ang. displacement in IVD y [ ]

4.5 L3/4
(Hayes et al. 1989; Li et al. 2009) report displacements in the same
L2/3
4 order; however, they measured flexionextension movements of higher
L1/2
3.5 amplitudes. Additional lines depict trend of values
3
2.5 and Panjabi (1990) present various in vivo measurements
2
of angular joint motion during flexionextension movement.
1.5
Interestingly, data presented in the literature do not match,
i.e. some present increasing angular motion from cranial to
1
caudal (Hayes et al. 1989; Ibarz et al. 2013; Pearcy and
0.5
Portek 1984; White and Panjabi 1990) while others present
0
0 2 4 6 8 10 12 14 16 18 the opposite (Lee et al. 2002; Li et al. 2009; Wong et al.
L[ ] 2004, 2006). The simulation results that were presented in
this study showed an increase in angular displacement during
Fig. 11 A Vertical displacements in the local sagittal plane (along the flexion in the order L1/2 (2.6 ) L2/3 (3.6 ) L3/4 (4.4 )
local longitudinal axis (z: caudocranial direction)) of the subjacent body
L4/5 (4.6 ). This caudocranial increase in angular IVD
and B angular displacements of intervertebral discs y in the local sagit-
tal plane of the subjacent body (its local xz-plane) as a function of the joint motion is in accordance with flexionextension studies
negative lumbar lordosis angle. Vertical and rotational displacements by Hayes et al. (1989), Ibarz et al. (2013), Pearcy and Portek
are depicted relative to displacement at tSET , i.e. rz,tSET = 0 m and (1984), White and Panjabi (1990): L1/2 (5 16 ) L2/3
y,tSET = 0 . Bold lines are used to emphasise translational and rota-
(7.8 18 ) L3/4 (6 17 ) L4/5 (9 21 ). Again, only
tional displacements in L4/5
relative changes could be presented (see Fig. 13).
Additionally, we compared our angular displacements
tant IVD forces again are compared with the literature data with the intervertebral flexionextension (IVFE) presented
(Fig. 11). by Lee et al. (2002), Wong et al. (2004, 2006). It indicates
Vertical displacements in the IVDs increase from cranial the relationship between net lumbar motion and motion of the
to caudal (top to bottom, see Fig. 12). For a simple flexion individual vertebrae. The IVFE is often used as input data for
movement simulated with our full human body model, the modelling of the IVD element in inverse dynamic models, cf.
displacement amplitudes increase from 0.34 mm (L1/2), to slope k in Christophy et al. (2011). Our presented joint kine-
0.45 mm (L2/3), to 0.58 mm (L3/4), to 0.62 mm (L4/5). In matics plotted against the lumbar lordosis angle are equiv-
vitro studies by Hayes et al. (1989) report displacements for alent to the IVFE. Our simulation results for the IVFE also
a complete flexionextension movement in the same order: show a linear-like pattern, like experiments determining the
L1/2 (1.9 mm) L2/3 (2.4 mm) L3/4 (2.5 mm) L4/5 IVFE characteristics. However, simulated IVFE in all joints
(3.0 mm). The same way, Li et al. (2009) report displacements of our model increase caudocranial, whereas in experiments
for a flexionextension movement in the order: L2/3 (0.2 IVFE slopes increase with investigated joints moving cranial.
0.2 mm) L3/4 (0.6 0.4 mm) L4/5 (0.7 0.6 mm). This is due to the fact that so far the new IVD model (Kara-
Additionally, the order of magnitude of all three studies lies jan et al. 2013) was used for all lumbar IVDs with the same
in the same range. parameters. The new, nonlinear IVD model was developed
More experimental data exist for the comparison of angu- for the L4/5 intervertebral disc and then applied to all other
lar displacements in the IVDs. Ibarz et al. (2013), White IVDs. We argue that by applying different scaled material

123
A forward dynamics simulation of human lumbar spine flexion

25
Pearcy et al. (1984) higher forces while standing and lower forces when reach-
Hayes et al. (1989)
Ibarz et al. (2013) ing a flexed position. Restoring forces during stance in the
range of ang. displacement in IVD []

White & Panjabi (1990)


20 our simulation Huynh model show good agreement with our model results,
while forces in flexion are underestimated.
15

Appendix 8: A simulation of heel impact with the


10 ground

We simulated a double heel contact of the model with the


5
ground after a free fall of about 8 mm, i.e. after about 0.04 s,
starting from a completely symmetrical initial position. To
0
L1/2 L2/3 L3/4 L4/5
insure ball contacts would not interfere with the impact, the
ankle joints were fixed in a slightly dorsally flexed orientation
Fig. 13 Angular displacements in the lumbar joints, w.r.t local joint as bracket joints, the latter being a method to set the number
coordinate system, increase from cranial to caudal. In vitro studies of degrees of freedom in a joint to zero. Just alike, we fixed
(Hayes et al. 1989; Ibarz et al. 2013; Pearcy and Portek 1984; White
and Panjabi 1990) report displacements in the same order; however, they the upper body to L1, resulting in a lumped L1-plus upper
measured flexionextension movements of higher amplitudes. Note, we body. Due to the stiffness 4 105 N/m of the linear elastic
did not include studies (Lee et al. 2002; Li et al. 2009; Wong et al. 2004, spring modelling the normal ground reaction force compo-
2006) with the opposite trend in this figure. Additional lines depict trend nent of each heel contact element, both heel elements were
of values
deformed about 2 mm in vertical direction during the impact.
The elements vertical damping force was modelled in pro-
properties and an enhanced IVD elements geometry, a more portion to the product of vertical deformation and velocity,
realistic IVFE pattern would occur. Additionally, it will fur- with the corresponding coefficient of proportionality set to
thermore result in a more physiological angular displacement 4105 Ns/m2 . Correspondingly, the net vertical ground reac-
behaviour. An enhanced nonlinear IVD model accounting for tion force reached a peak of about 65 m/s2 (Fig. 14).
the mentioned shortcomings is already available, but was not The mass distribution in the model was chosen such that
ready to be included in this study yet (Karajan et al. 2014). all segment masses represented just the bony parts. This is
In vivo measurements of lumbar joint dynamics are rare. because it is only the skeleton that is decelerated during this
For a first validation, we used intradiscal pressure measure- impact period of about 20.0 ms (Denoth et al. 1985; Nigg and
ment data of the IVD L4/5. Measurements were taken with Denoth 1980), whereas all soft tissue material like the mus-
one healthy male test subject in different postures by Wilke cles is coupled viscoelastically to the bones (Denoth 1985;
et al. (1999, 2001). They measured a disc pressure of 0.43 Gruber et al. 1998; Gnther et al. 2003; Schmitt and Gn-
0.5 MPa during relaxed standing of the test subject (body ther 2011) and decelerated with a time delay. In modelling
mass 70 kg, body height 1.74 m). In a 36 flexed standing pos- its mechanical response, the soft tissue material is denoted
ture, the disc pressure increased almost linearly to 1.08 MPa. wobbling mass (Denoth 1985). The ratio of wobbling to
The flexion angle was defined differently, i.e. between the segment mass was set to zero in the feet, to 1/2 in the shanks,
thoracolumbar junction and the sacrum (fl,S1T12 ). The and to 2/3 in the thighs (Gnther et al. 2003; Schmitt and
disc area, measured using magnetic resonance imaging, was Gnther 2011). For the pelvis bony part, we assumed 3.0 kg,
18 cm2 . Thus, the respective axial joint force was 774900 N neglecting an assumed wobbling mass portion of 5.3 kg. The
in relaxed standing and 1,944 N in a flexed position. In our bony masses of the 24 vertebrae were assumed to decrease
model, axial forces increased from Fz,upright = 942 N dur- from about 50 g in L5 to 10 g in C1. In our model, the inertia of
ing upright stance to Fz,flex = 1,681 N at tsim,end-nl with all vertebrae from T12 up to C1 is included in the upper body.
fl,S1T12 = 3 and fl,S1T12 = 33 , respectively. Taking For the upper body, we applied the effective mass concept
into account our slightly different flexion angle (higher at the introduced by Denoth (1986), Denoth et al. (1985): during
beginning, smaller at the end), simulated longitudinal forces the 20.0 ms impact period, the effectively decelerated mass
using the nonlinear IVD model in L4/5 show good agreement may depend on both net bony mass of the body and the ini-
with experimental data. tial joint angular configuration. We estimated that one-third
In comparison with in vivo measurements of joint dynam- of the 36.8 kg act effectively during impact. Altogether, the
ics (Wilke et al. 1999, 2001), our new, nonlinear IVD model decelerated body masses summed to 25.0 kg in our impact
included in the spine model shows the best agreement (see model.
3.1). The classical, linear IVD model variations using either The resulting distribution of vertical acceleration compo-
Monteiro parameters or GardnerMorse parametres result in nents measured in the global reference frame is plotted in

123
T. K. Rupp et al.

120 shank time along the vertebral column comprising 24 IVDs, we


100
foot
thigh
found 24 0.734ms 4.4 ms. The deviation from the data
pelvis by Lafortune et al. (1996) can be easily explained by two
body acceleration [m/s 2 ]

80
L5 delaying contributions missing in our model so far: (1) those
L4
60 by the cartilage in the leg joints and (2) those by acoustic
grf
40 L3 wave propagation in the bones. However, the latter effects
L2
20 L1 should be negligible because the elastic modulus of bones is
about 4 orders of magnitude higher than that of IVDs, with
0
approximately the same mass density.
20 The distance between L5 and C1 is roughly 60 cm. Thus,
40 we can estimate the propagation velocity from our computer
experiment to be clong = 60 cm/4.4 ms = 136 m/s. Based
0.04 0.045 0.05 0.055 0.06 0.065 0.07
on theory, we may predict this number based on elastic mod-
time [s]
ulus E = = Fl Al00 with the stress = A0F , the strain
Fig. 14 Vertical components of the models net ground reaction force = l0l , and the stiffness K = Fl . The area of a verte-
and each segments centre of mass acceleration during an impact of the
upright model on the heels from 8 mm falling height bras upper endplate is roughly 1 cm2 and the range of IVD
thicknesses is about 1 cm. . .0.5 cm from L5 to C1. In gen-
eral, wave propagation velocity clong in solids depends also
Fig. 14. There is a shock wave propagating from the feet to
the head. The acceleration amplitudes decrease from distal to on the Poisson ratio = A0A / l0l . For longitudinal waves,

proximal in the legs, with a slight deviation from this rule: the E(1)
theory predicts clong = (1 2 ) , where symbolises
foot acceleration is a little lower than the shank acceleration.
This fact is due to the foot centre of mass being located about the mass density. With a lumbar IVD stiffness estimation of
10 cm anterior to the ankle and its upward movement deter- 5 105 N/m (compare Table 2), lumbar thickness of 1 cm,
mined by a superposition of heel translation and footshank and a small Poisson ratio 0.5, a value of clong = 73 m/s
rotation. Above the pelvis, the amplitudes decrease along the can be predicted from theory. This is nearby the theoretical
lumbar spine from caudal to cranial. Quantitatively, the accel- minimum value for = 0. This theoretical clong increases
eration maxima are time-shifted according to the following for approaching the pole 0.5. For = 0.45, clong would
segmental sequence: shank(s) (0.06 ms), thigh(s) (0.02 ms), be about twice the minimum value.
pelvis (0.01 ms) L5 (0.08 ms) L4 (0.26 ms) L3 (0.18 ms),
whole body (0.22 ms) L2 (8.73 ms) L1-plus upper body. The
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