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DOI 10.1007/s10237-015-0656-2
ORIGINAL PAPER
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 ( )
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)
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.
2.6 Simulation
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A forward dynamics simulation of human lumbar spine flexion
0
3 Results
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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
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
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-
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A forward dynamics simulation of human lumbar spine flexion
A 20
RA
A 25
nl
EO 20 lGM
F M /Fmax (sum of fascicles) [%]
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) [%]
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.
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T. K. Rupp et al.
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A forward dynamics simulation of human lumbar spine flexion
1000
(2010) used the lumped stiffness parameters to model the
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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
200
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.
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 )
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 )
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 )
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)
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)
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)
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
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 []
123
T. K. Rupp et al.
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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