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Biomechanics of Musculoskeletal System and


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Journal of Bionic Engineering 11 (2014) 159175

Biomechanics of Musculoskeletal System and Its Biomimetic


Implications: A Review
Lei Ren1,2, Zhihui Qian2, Luquan Ren2
1. School of Mechanical, Aerospace and Civil Engineering, University of Manchester, Manchester M13 9PL, UK
2. Key Laboratory of Bionic Engineering (Ministry of Education, China), Jilin University, Changchun 130022, P. R. China

Abstract
Biological musculoskeletal system (MSK), composed of numerous bones, cartilages, skeletal muscles, tendons, ligaments
etc., provides form, support, movement and stability for human or animal body. As the result of million years of selection and
evolution, the biological MSK evolves to be a nearly perfect mechanical mechanism to support and transport the human or
animal body, and would provide enormously rich resources to inspire engineers to innovate new technology and methodology to
develop robots and mechanisms as effective and economical as the biological systems. This paper provides a general review of
the current status of musculoskeletal biomechanics studies using both experimental and computational methods. This includes
the use of the latest three-dimensional motion analysis systems, various medical imaging modalities, and also the advanced
rigid-body and continuum mechanics musculoskeletal modelling techniques. Afterwards, several representative biomimetic
studies based on ideas and concepts inspired from the structures and biomechanical functions of the biological MSK are discussed. Finally, the major challenges and also the future research directions in musculoskeletal biomechanics and its biomimetic
studies are proposed.
Keywords: musculoskeletal system, biomechanics, multi-scale, biomimetics, biologically inspired robots and mechanisms
Copyright 2014, Jilin University. Published by Elsevier Limited and Science Press. All rights reserved.
doi: 10.1016/S1672-6529(14)60033-0

1 Introduction
A musculoskeletal system (MSK) is a biological
system composed of bones, cartilages, skeletal muscles,
tendons, ligaments and other connective tissues (see
Fig. 1). The major function of the MSK is to provide
form, support, movement and stability for the human or
animal body. The MSK can be roughly considered to
have two constituent sub-systems: the skeletal system
and the muscular system.
The skeletal system consists of all the bones in the
body and also the connecting tissues, e.g. cartilages and
ligaments. The skeletal system provides the fundamental
framework for body shape and load bearing, and also
protects internal organs, e.g. brain, heart, lungs and liver
etc., from external impacts. In the skeletal system, bones
are connected to each other by joints, which provide
articulations in MSK. The most common type of joint is
synovial joint, which consists of fibrous connective
tissue capsule (ligaments) and the periosteum of the
Corresponding author: Lei Ren
E-mail: lei.ren@manchester.ac.uk

connecting bones lubricated by synovial fluid inside of


the joint.
The muscular system is the prime mover of human
or animal body. For humans, there are approximately

Fig. 1 The musculoskeletal system of human body[1].

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Journal of Bionic Engineering (2014) Vol.11 No.2

over 430 skeletal muscle groups accounting for up to


40% of body weight[2]. The skeletal muscles are made up
of hundreds, or even thousands of muscle fibers, which
range in thickness from approximately 10 m to 100 m
and in length from about 1 cm to 30 cm[2]. Skeletal
muscles are also arranged in layers over the bones, and
they are normally attached to bones through tendons so
that the forces generated by the contractile elements of
the muscle fibers can drive body motions.
As the result of million years of selection and evolution, the biological MSK evolves to be a highly efficient and economic mechanical mechanism to support
and transport the human or animal body with many extraordinary characteristics compared to their man-made
counterparts. For example, cheetah is known as the
fastest living land quadrupedal animal, which can reach
to a speed of 29 ms1[3]. Some special features of cheetahs MSK have been reported probably contributing to
attaining such a high speed. For example, their divergent
talar ridges may help to avoid limb interference in the
aerial phase of galloping. Their long hindlimb bones
may potentially assist them in making large stride length.
Moreover, their particularly large psoas muscles may
help them to rapidly protract the hindlimbs and also to
resist pitching moments around the hip during accelerating[4]. Another example is horses, a representative
athletic ungulate land animal with excellent locomotor
capacity. Their third metacarpus bone has a small hole
where blood vessels enter the bone[5]. As common
knowledge from mechanical engineering, holes normally weaken structures by increasing dramatically the
stresses near the holes as a result of stress concentration[5]
(see Fig. 2). However, the holes at the third metacarpus

bones of horses do not appear to cause bone fractures


even for racing horses. This is probably due to an increased compliance near the foramen[5]. The sharp discontinuity in geometry due to the hole is softened by an
embedded compliant region[5]. A reinforcing ring with
increased stiffness, together with the ring of lamellar
bone along the foramens inner edges, might help to
reduce the possibility of cracking[5]. The special configuration of the hole helps to move the highest stresses
away from the foramen to regions with higher material
strength[5] (see Fig. 2).
The human foot complex is another good example
of highly efficient mechanical mechanism from the
biological world. The human foot is a complicated
structure comprising numerous bones, muscles, tendons,
ligaments, synovial joints and other tissues. It has been
found recently that such a small body component delivers multiple critical biomechanical functions in attenuating ground impact, supporting body against gravity, maintaining locomotor stability, generating and
transmitting propulsive power during locomotion[68].
The fascinating structure and characteristics of the
biological MSK, which has been optimally selected after
million years evolution, would provide enormously rich
resources to inspire engineers to innovate new technology and methodology to develop mechanisms and machineries as effective and economical as the biological
systems. For example, legged locomotion, as a biological transportation solution over rough terrain, has been
attracting intensive researches from mechanical engineering and robotics field[913]. This may greatly facilitate the development of legged robots with high agility,
stability and energy efficiency.

= 1.5 MPa

Fig. 2 The foramen in horse third metacarpus bone and its stress analysis[5].

Ren et al.: Biomechanics of Musculoskeletal System and Its Biomimetic Implications: A Review

This paper starts with a brief introduction of the


MSK and the biomechanics of its constituent components. Afterwards, a general review of the current status
of the MSK biomechanics, including both experimental
and computational studies, is provided. Several representative biomimetic examples based on inspired ideas
from MSK biomechanics are discussed. Finally, the
major challenges and also the future research directions
in MSK biomechanics and its biomimetic studies are
proposed.

2 Experimental studies of MSK biomechanics


2.1 Motion capture
In the past decades, motion capture technique has
been increasingly used in recording the two-dimensional
(2D) or three-dimensional (3D) human/animal motion,
which is characterized by the time histories of segmental
or joint angles. Generally, optoelectronic motion analysis systems are employed by using infrared camera arrays to track the positions of active or passive markers
placed on the body segments of interest[1422] (see Fig. 3).
Although the optoelectronic motion capture technique
has now been widely used in human/animal movement
studies, the collected data normally suffer from some
technical problems, e.g. skin artifact (due to the relative
movement of skin mounted markers with respect to the
underlying bones)[16,2325], light reflections and marker
occlusions[26]. Markerless motion tracking method based
on computer vision provides a new promising motion
capture technique[27]. Currently, the markerless systems
can work with large, obvious movements, while the
measure of more subtle movements still remains chalHead

Torso

Humerus
Forearm+hand

Thigh
Pelvis
Shank

X
K
Fgl

161

lenging.
To complement the motion capture, many biomechanics labs are also equipped with force sensing devices to record the simultaneous kinematic and kinetic
data associated with human/animal motions. 3D force
platforms are normally used to measure the ground reaction forces and moments induced by human/animal
motions. Integrated with the simultaneous motion data,
joint kinetic analysis can normally be conducted by
using the inverse dynamics method[17,2830]. Additionally,
pressure plates are often employed to record the foot
pressure distribution during human/animal motions[3134].
In addition to multi-camera systems, portable motion
sensors are also used to capture human/animal body
motions, e.g. inertia sensors (i.e. accelerometers, gyroscopes etc.) and magnetometers etc.[3538]. This offers an
alternative way to measure the human/animal motions
outdoors without the constraints of the indoor equipments[39,40].
2.2 Surface electromyography
Human or animal electromyography signals at different motor activities can be recorded using invasive or
non-invasive methods. Surface electromyography
(sEMG) is a non-invasive technique widely used for
detecting and recording muscle electrical activity that
occurs during muscle contraction and relaxation cycles
by using surface electrodes. The sEMG signal is normally used in musculoskeletal biomechanics studies as
an indicator of the initiation of muscle activation, as an
estimator of the force produced by a contracting muscle,
or as an index of the fatigue occurring within a muscle[28,41,42]. In other words, sEMG signals may contain
information about whether a muscle is active or not, if a
muscle is more or less active, when it is on and/or off,
and also if it fatigues[43]. However, raw sEMG data may
contain mixed electrical signals from multiple muscles
nearby the electrodes and/or noisy signals due to
movement artifact, so dedicated signal processing is
normally needed before useful information can be obtained to interpret the muscle functions[28,44,45].

Foot
K
M gl

K
M gr

K
Fgr

Fig. 3 The three-dimensional whole body model with 13 segments and 12 connecting joints. A specially designed marker
cluster system mounted on plastic plates was used to capture the
segmental motions[17].

2.3 Medical imaging


Medical imaging domains, e.g. Computed Tomography (CT), Magnetic Resonance Imaging (MRI), ultrasound, are very useful techniques to examine the
anatomy, geometry and structure of a MSK. Among

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Journal of Bionic Engineering (2014) Vol.11 No.2

them, the ultrasound provides an economic noninvasive


imaging technique by transmitting high-frequency
sound waves through a body part. As a handy diagnostic
tool, ultrasound has been widely employed in musculoskeletal biomechanics studies to investigate the in vivo
muscle structure, muscle fiber movement, neuromuscular disorders etc.[4649]. Although superficial muscles
may be easily detected by ultrasound probes, it is difficult to identify individual small muscles when multiple
muscle groups are involved[50]. Additionally, due to the
reflection or absorption of sound by superficial tissue
layers, it is still challenging for ultrasound to detect
deeper muscles especially in the pelvic region or around
the trunk. Since ultrasound has difficulty in penetrating
bones, to examine the structure of bones, or a particular
musculoskeletal complex, e.g. certain joints or body
segments, other imaging modalities, such as CT and/or
MRI, are generally used.

3 Biomechanical MSK modelling


3.1 Rigid body modelling of MSK
Rigid body dynamics is typically used to simulate
human/animal motions by considering the body segments of interest as rigid bodies without any deformations. Over the past decades, numerous rigid body
models have been developed to simulate human/animal
movements or motions of particular body parts with
varying complexity from simple one-segment model
with 1 DOF to complex model with 10 segments and 23
DOFs[17,5166] (see Fig. 4). In those models, the con-

Fig. 4 A large-scale musculoskeletal model with 23 generalized


DoFs and 54 musculotendon actuators[61].

necting joints are typically defined as frictionless


ball-and-socket joints, hinge joints or universal joints.
Whilst the mechanical behaviour of muscles was normally represented using Hill-type models[56,66,67], where
the normalized muscle force of the contractile element is
the product of three independent experimentally measured factors describing the force-length property, the
force-velocity property and the dynamics of neural activation[56,57]. Model simulations can be applied in two
different ways, which are usually referred to as the
forward (direct) dynamics method, and the inverse dynamics method. In the forward dynamics method, the
motions of the segments are determined by integrating
the equations of motion based on predefined joint moment or muscle force/activation data[53,61,65,66,68,69]. In the
inverse dynamics method, the joint forces and moments
are determined based on the measured joint or segment
motion data[17,2830,66].
Biomechanical analysis based on rigid body models
can be applied to a wide range of problems, such as the
assessment of the effect of tendon transfer surgeries[6971],
the investigation of multi-segment interaction[72,73], the
musculoskeletal performance during walking and
jumping[65,68,7476], the development of neural prostheses[77], the neural control principles of movement[7880],
the effect of musculotendon loss or damage on the
overall joint moment capacity[81], and the effect of load
carriage design on walking performance[82]. Recently,
several software packages have been developed for rigid
body musculoskeletal model construction, simulation
and analysis, e.g. SIMM[69], OpenSim[83], AnyBody[84],
MSMS[77] etc., which normally provide graphical user
interface for general users.
Despite the recent great progress and success, there
are still some major unsolved problems in rigid body
musculoskeletal modelling. Firstly, the anatomical joints
are typically simplified as ideal ball-and-socket or hinge
joints to reduce computational load, which are not realistic representations of most biological joints. In addition, there are still a large amount of works needed to
improve the in vivo representation of musculotendon
mechanics and neural dynamics, especially on a subject-specific basis. Finally, the development of predictive musculoskeletal models, which are capable of predicting kinematic and kinetic variables during motions
with minimal measurement inputs, still remains as a very
challenging task[61,66,85].

Ren et al.: Biomechanics of Musculoskeletal System and Its Biomimetic Implications: A Review

3.2 Continuum mechanics modelling of MSK


Over the past decades, methods based on continuum mechanics, e.g. Finite Element (FE) method,
boundary element method etc., have been increasingly
used to investigate the mechanical behaviour of musculoskeletal structures by considering constituent components as deformable bodies. The FE method is a very
useful numerical tool to handle biological structures
normally with highly non-linear material properties,
irregular geometries and complicated boundary conditions. Recently, the FE method has been widely used in
biomechanical studies of MSK, covering a broad range
of topics, e.g. functions of musculoskeletal complexes,
mechanics of joints and skeletal muscle mechanics etc.
3.2.1 FE modelling of musculoskeletal complexes
The FE method has been particularly useful to investigate the mechanical behaviour of specific musculoskeletal complexes of the human body, normally
comprising numerous bones, joints and soft tissues, e.g.
the spinal column or the ankle-foot complex. Substantial
FE studies have been conducted on the biomechanics of
cervical vertebrae, thoracic vertebrae and lumbar vertebrae. Some earliest works involves the modelling of the
cervical spine and the lumbar vertebral motions[8690].
Saito et al. constructed a spine model to analyze the
prevention of spinal column deformity with oversimplified representation of vertebral geometry and the inter-vertebral joints, which may lead to an unrealistic
assessment of load sharing and stress distributions[91].
The model may be suitable for the study of gross responses of the whole column rather than the local
changes at the individual vertebrae level. Kleinberger
presented a sophisticated model including head and
various spinal components for FE analysis[92]. However,
the model lacked sound representations of the anatomical structure of the spine probably because the major aim
of the study was for crash impact analyses rather than
medical applications. The three-segment lower cervical
spinal unit model constructed by Voo et al. had a reasonable representation of the cervical anatomy based on
CT scans and cryomicrotome anatomical sections[93,94],
which could be extended to the construction of the entire
cervical column. Most of the FE studies of spinal column are based on static analysis[9597]. Although internal
stresses, strains and other biomechanical responses under complex loading conditions could be predicted, they

163

provide very little information about the in vivo condition of the whole column during dynamic motions.
Whereas some FE models consisting of a series of
connected vertebrae could predict the dynamic responses of the spine to external loads[98,99]. Zhang et al.
constructed a detailed cervical spine model (C0-C7)[100].
The predicted biomechanical response of human neck
under physiological loadings, near vertex drop impact
and rear-end impact conditions, were analyzed and
compared with published measurement data, demonstrating potential for future biomedical and traumatic
studies.
The human foot is a very complex structure comprising numerous bones, joints and soft tissues, delivering a variety of biomechanical functions during human
motions. Over the past decades, a large number of studies
based on FE method have been conducted to investigate
the biomechanical functions of the foot complex. Lemmon et al. used a 2D FE model to study the effect of
insoles on therapeutic footwear based on quasi-static
simulations[101]. Patil et al.[102] conducted a stress distribution study on normal and neuropathic feet during gait
using a 2D model, which was constructed from a lateral
X-ray image. Wu[103] constructed a 2D FE model to study
the foot bone and muscle stresses resulting from plantar
fasciotomy and major plantar ligament injuries. Chu et
al.[104] conducted a static parametric analysis using an
asymmetric 3D FE foot model to investigate the ankle-foot orthosis effects by considering the foot complex
as a single segment. Jacob et al.[105] developed a 3D FE
model with the purpose being to investigate the contributing factors to disintegration of tarsal bones in Hansens
disease and diabetes. Gefen et al.[106] constructed a subject-specific 3D foot model based on realistic bone geometry to investigate the biomechanical foot function
during gait. The stress distribution analysis was conducted at six representative instants of time during gait.
Gefen[107,108] also developed a 2D FE model to investigate the foot biomechanics following surgical plantar
fascia release and also to evaluate the plantar stress distribution of a standing diabetic foot. Cheung et al.[109111]
developed a more complicated 3D foot model by using
realistic bone geometry and nonlinear material properties.
The model was used to investigate the effects of plantar
fascia stiffness and Achilles tendon loading, and also to
conduct the parametric design using different structural
and material properties of a foot orthosis. Recently, the

Journal of Bionic Engineering (2014) Vol.11 No.2

164

foot plantar fascia mechanics, stress concentration in


plantar soft tissues and also the load transfer mechanism
were analyzed using different 3D FE foot models[112116].
However, it is noteworthy that almost all these studies are
static or quasi-static in nature. So far, very few foot
biomechanics studies used dynamic FE analysis. Dai et
al.[117] used a 3D foot model to investigate the effect of
sock wearing on the plantar pressure under different
contact conditions from the foot-flat to the push-off
during the stance phase of gait based on dynamic FE
simulations. However, constant loads were assumed and
extra constraints were used to define the model, which
may lead to unrealistic motion of the foot complex. Very
recently, a fully dynamic foot model without any extra
constraints has been developed to simulate the dynamic
behaviour of the human foot structure during stance
phase of walking, which has demonstrated some advantages over the traditional static or quasi-static FE models[118] (see Fig. 5).
3.2.2 FE modelling of musculoskeletal joints
The FE method has also been extensively used to
investigate the joint mechanics, especially the contact
stress and strain responses of different joint components.
Brown and Digioia[119] used a 2D FE model to analyze

t = 0 (s)

t = 0.03 (s)

t = 0.19 (s)

t = 0.23 (s)

t = 0.40 (s)

t = 0.44 (s)

the articular contact at hip joint, by representing the


cartilage using non-linear contact elements. An
axis-symmetric FE model of meniscus was proposed
with non-linear material properties, and the simulation
results suggested high radial strains in the regions where
lesions were most often observed[120]. Eckstein[121] used
the FE model to analyze the stress distribution at elbow
joint, and found that incongruity generates advantageous
mechanical stimuli in the joint tissues. The FE method
was also applied to the shoulder mechanism by using
truss, hinge and surface elements to construct the
model[122]. Sophisticated FE models of the knee joint
were also reported to study the meniscus and the contact
condition between cartilage and meniscus[123125]. In
addition to cartilages, ligaments are also important
components of a musculoskeletal joint. Usually, 1D
element was employed to represent ligaments in FE
modelling of joints. The 1D representation requires only
few parameters to define the mechanical behaviour. This
approach was proved useful for predicting joint kinematics under the application of external loads[126]. But it
has some shortcomings: (1) non-uniform 3D stresses and
strains cannot be predicted; (2) multiple sets of parameters and initial tensions routinely produce nearly
identical predictions of joint kinematics[127]. Ligaments

t = 0.08 (s)

t = 0.27 (s)

t = 0.43 (s)

t = 0.45 (s)

Fig. 5 The von Mises stress distribution predicted by a dynamic finite element foot model at 10 representative instants of
time over the whole stance phase of human walking[118].

Ren et al.: Biomechanics of Musculoskeletal System and Its Biomimetic Implications: A Review

are subjected to highly non-uniform deformations in vivo


that result from a combination of tension, shear, bending,
and compression[128,129], and the regional contribution of
a ligament to joint stability changes with joint orientation[130,131]. Therefore, 3D FE modelling is desirable to
represent these mechanical characteristics[132134]. The
FE modelling of musculoskeletal joints offers a useful
tool to predict the spatial and temporal variations in joint
contact stresses and strains, which are difficult or impossible to obtain experimentally.
3.2.3 FE modelling of skeletal muscles
As the prime mover of the MSK, skeletal muscles
demonstrate very complicated mechanical properties
coupled with neural excitations and muscle fibre contractions[135,136]. Currently, most of the mathematical
representations of muscle contraction mechanics are
based on either Hills model or Huxleys theory[137140].
Hills model depicts the dynamics of a musculotendon
unit using a set of connected discrete mechanical elements. This could help stimulate some initial schemes
toward a simple FE model of skeletal muscles[141].
Some initial works on FE modelling of skeletal
muscles involved the representation of muscle-tendon
complex using a number of simple active 1D line elements, each of which is composed of motor and viscoelastic elements. Since the 1D line elements did not
have volumes and masses, the information about muscle
tissue stresses and inertia effects could not be obtained.
Moreover, the muscle moment arms were assumed to be
equivalent for all fibres within a muscle compartment.
This limits the ability of the model to accurately represent the actual paths of muscles with complex geometry
and also the stress response of the active part and passive
part individually. A 3D FE muscle model has the potential to represent the complex muscular structures and
improve our understanding of the musculotendon mechanics[58]. Since a skeletal muscle consists of contractile muscle fibres arranged within a passive matrix of
connective tissues[142], a number of FE models have been
developed to describe the active behaviours of skeletal
muscles. Tsui et al.[143] constructed a 3D active FE
muscle model by using a user-defined muscle behaviour.
The simulation results of isometric force-length relationship and force-shortening contraction demonstrated
the potential of the model for studying muscle damage
and fatigue. Tang et al.[140] developed a 3D FE model of

165

skeletal muscles by integrating a modified Hills muscle


model with a muscle fatigue formula, but neglected the
different fibre types inside of the muscle. Based on the
two-state Huxley model, Oomens et al.[144] constructed a
3D muscle model to estimate the inhomogeneous strain
distribution in a skeletal muscle. A good agreement
between the measurement data and the simulation result
showed the proposed model could be employed as a tool
for studies on damage and adaptation of skeletal muscles.
Different from the mechanical properties during active
conditions, the passive muscle behaviour was normally
represented by non-linear hyperelastic or viscoelastic
constitutive relationship in the FE modelling of the
skeletal muscle[140,145,146] (see Fig. 6).
Due to the highly anisotropic, nonlinear material
property, and also the complex geometry (multiple layers
of soft tissue) and boundary conditions, 3D FE modelling
of stress-strain behaviour of skeletal muscles is normally
complicated and computationally demanding. The traditional solutions for FE simulations based on standard

Extended

Flexed

Fig. 6 The reconstructed 3D muscle models of gluteus maximus,


gluteus medius, iliacus, psoas by segmentation of MR images[146].

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Journal of Bionic Engineering (2014) Vol.11 No.2

non-linear FE formulations are time-consuming even for


one or two muscles[147]. Blemker et al.[148] developed a
quasi-static invertible FE algorithm to reduce the computational load, which provided two major improvements over the traditional methods: (1) elements are
allowed to invert by computing robust FE forces with a
invertible framework; (2) the stiffness matrix is positive
semi-definite.
Nowadays, mathematical models representing the
mechanical behaviours for muscle-tendon complexes
used for studying the dynamics of the human MSK are
dominated by various Hill-type models[149151]. The development of bio-realistic and computationally efficient
FE models of the muscular system for assessing the
dynamic functions of biological MSK is still at its very
early stage.

4 Biomimetic studies inspired by MSK biomechanics


4.1 Bioinspired quadrupedal robot - BigDog
BigDog is a dynamically stable quadrupedal robot
developed by Boston Dynamics[152], with aim being to
provide load carriage service to accompany soldiers in
harsh rough terrains, which are impossible for conventional vehicles with wheels or treads. The size of the
robot is of a large dog or a small mule, about 1.1 m long
and 1 m tall, and weighs 109 kg. The robot has four legs
that are articulated like a typical quadrupedal animal,
with compliant elements to absorb shock and store energy during moving. It is capable of performing a variety
of locomotion behaviours, such as walking, running,
climbing, jumping and carrying heavy loads in
rough-terrain conditions[152].
Ideas and concepts inspired from quadrupedal
animals have been used in the structure and actuation
design, sensor and motion control of the BigDog robot.
The single leg structure, in terms of joint configuration,
standing posture and actuator position, is very similar to
the leg of a typical quadrupedal animal (see Fig. 7).
Going distally from hip joint to metatarsal joint, the leg
actuation of a typical quadrupedal animal becomes less
strong, and contains more compliance. In addition, the
forelimb and hindlimb configuration of the BigDog uses
similar design principle of the four-legged configuration
in horses, dogs and goats[153,154]. As the compliant
components of animals MSK play important role during
dynamic moving, such as running, jumping and gallop-

Fig. 7 The bio-inspired back leg of the BigDog robot compared


to the hindlimb of a typical quadrupedal animal[152].

ing[155], spring components are integrated into the leg of


the BigDog to attenuate the ground impact during dynamic moving (see Fig. 7). When moving on the ground,
the joint position, joint force, ground contact, ground
load and external obstacles of the robot are monitored by
using onboard sensors to ensure its dynamic balance and
stability. The robot could also behave like quadrupedal
animals to adapt to the local terrain variation by adjusting its body height and attitude, and also foot placements.
Based on those bio-inspired ideas and concepts, the
BigDog exhibits excellent locomotion performance, e.g.
it can climb slopes up to 35 degrees, walk across rubbles,
climb muddy hiking trails, walk in snow and water etc.
So, the BigDog has been considered as one of the most
advanced quadrupedal robots moving on rough terrains[152].
4.2 Efficient human-like robot with compliant legs
Over the past decades, many bipedal robots
have been developed to mimic human locomotion[10,12,13,156163]. Most of those walkers used precise
control to regulate the angle values of each individual
joint at each instant of time during locomotion. This
requires actuators with high precision and frequency
response, a precise environment model and also high
energy cost[10,12,13]. Recently, the concept of passive
dynamic waking, which needs less actuators and active
control than mainstream robots, was proposed as a new
design and control paradigm[159162,164]. It has been
demonstrated that periodic stable walking can be
achieved with high energy efficiency and little control
by integrating simple actuations into passive dynamic
walkers[160].

Ren et al.: Biomechanics of Musculoskeletal System and Its Biomimetic Implications: A Review

A recently developed bipedal robot based on the


passive dynamic walking concept, used minimum control to drive two elastic legs inspired from the structure
of the human leg MSK[164]. The robot consists of seven
body segments, two servomotors at the hip joints, four
passive joints at knee and ankle joints, and totally eight
linear springs (see Fig. 8). The spring components were
used to mimic the passive mechanical function of the
major musculotendon units in human legs. A unique
feature of the robot is that it has six springs spanning
over two joints to mimic the major biarticular muscles in
the leg. The experimental study showed that this
bio-inspired bipedal robot could produce human-like
walking gait by using extremely simple control without
sensory feedback[165]. This is a good example for development of bipedal robots with higher energy efficiency and more natural walking pattern based on ideas
inspired from the biological structure of the MSK.
(a)

(b)
Hip motor
Springs

Passive joints

Rubber

(c)

Fig. 8 The human-like bipedal robot with compliant legs[165]. (a)


bipedal robot model, only one leg is shown; (b) schematic of the
robot design; (c) the physical robot platform.

167

5 Challenges and future directions


The last decade has seen great progress and advance in the human/animal movement studies, which
aim for understanding the biomechanical functions of
the biological MSK using both experimental and computational approaches. However, due to the great complexity of the biological MSK, there still remain many
unsolved problems and grand challenges in musculoskeletal biomechanics. Skin artefact has been the major barrier for 3D motion analysis systems to become a
useful clinical diagnostic tool. X-ray based video systems (e.g. fluoroscopic systems) may be helpful to reduce the skin artefact during motion capture[166168], but
the effect of radiation and the limited measuring volume
prevent it from being useful in general cases. Assessment of individual muscle forces in vivo during human/animal motions has been proven to be a grand
challenge in musculoskeletal biomechanics field[169171].
Due to the limitation of the current measuring techniques and ethical reasons, the direct measurement of the
in vivo musculotendon forces is almost impossible. So,
rigid body musculoskeletal modelling technique is
normally used together with optimisation algorithms to
estimate the muscle forces that can reproduce measured
joint motions. However, the determination of the subject-specific muscle parameters, musculoskeletal geometry and the rigorous experimental validation of the
calculated results still remain big challenges[172]. In addition, development of predictive musculoskeletal
models, which are capable of predicting body kinematics and kinetics during various movements with minimum measurement inputs[61,66,85], will be one of the
major future research directions due to their great potential in clinical diagnosis, rehabilitation engineering
and surgical planning.
In musculoskeletal biomechanics studies, computational FE modelling provides a unique tool to assess
the internal stress/strain conditions of the biological
MSK, which is normally not measurable in vivo. Properly conducted FE studies could help to investigate the
fundamental biomechanical mechanisms of the MSK, to
improve our understanding of the associated musculoskeletal disorders, and hence to provide sound scientific basis to facilitate clinical diagnosis and surgical
treatments. One of the challenging works in FE modelling of MSK is to provide accurate definitions of the in

168

Journal of Bionic Engineering (2014) Vol.11 No.2

vivo material properties of the soft tissues and hard tissues in MSK. For example, the definition of the constitutive equation of cancellous bones is still a subject of
debate, in particular those relating to post-elastic behaviour[173175], and the failure criteria[176,177]. Similarly,
there are also lacks of accurate definitions for the in vivo
material properties for the soft tissues (e.g. cartilages,
ligaments, tendons and muscles etc.).
Another challenging work in FE modelling of MSK
is to provide bio-realistic representations of the anatomy,
structure and function of the human MSK at different
levels/scales (e.g. organ level, tissue level and cell level).
As we know, mechanical loadings at macro level have
effect on behaviours at micro level, conversely mechanical properties at micro level influence system responses at macro level[178]. For example, diabetic foot
ulceration may have a biomechanical etiology[179]. For
patients with diabetes, some common daily activities,
e.g. walking, may be harmful because diabetes may
affect the biological functions of MSK at various levels.
Dysfunctions at different levels manifest themselves in
terms of loss of sensation[180], changes in control of
movement[181], and alteration of tissues[182] and also cell
properties[183]. It is unclear how do mechanical loads at
macro level (e.g. ground reaction forces) response to
cellular deformations that may cause cell damage or
even ulceration. Mechanical loadings at macro level (e.g.
increased foot contact pressures), redistribution of stress
due to changes in tissue composition (e.g. muscular
atrophy[184], cell distribution within tissues, increased
mechanical loading of cells or their decreased damage
resistance may all have contributions to the development
of ulceration. Therefore, a multi-scale modelling
framework is needed to identify the pathways to cell
damage from the mechanical loadings at organ level
through to the deformations at cell level.
Multi-scale modelling has been used in basic science and engineering areas e.g. mathematics, material
science, chemistry and fluid dynamics etc. for many
years. When applied to MSK biomechanics, the
multi-scale modelling approach is normally based on an
integrated hierarchical structure at multiple body levels,
where the mechanical outputs of macro level models are
transmitted to micro level models with detailed representations of MSK at tissue and cell level[185]. Normally,
rigid body dynamics is used to simulate the mechanical
behaviour of MSK at body level, and continuum me-

chanics is employed to represent the stress-strain interplay at organ level, whereas for simulations at tissue and
cell levels specialized algorithms and solvers are normally needed[178,185]. Therefore, multi-scale MSK
simulations are computationally intensive, and require
intricate representations and also effective simulation
strategies/approaches to describe the complex interactions among multiple levels.
After multi-scale MSK simulations are conducted
to address specific research problems or particular
clinical questions, the next challenging stage is to interpret and validate the simulation results. It is a very
daunting and time consuming task to interpret the complicated calculation outcomes obtained or to extract
clinically meaningful information from the huge amount
of database generated by the multi-scale simulations.
Moreover, the lack of in vivo subject-specific data (e.g.
muscle forces, mechanical properties of hard and soft
tissues etc.) and the complexity associated with experimental measurements make the validation of the
simulation results even more challenging[178]. Although
parameter sensitivity studies coupled with statistical
populations of in vivo and primarily in vitro data may
provide some initial verifications, the limitation of the
current measuring techniques make a thorough subject-specific in vivo validation impossible. Furthermore,
the highly demanding nature of clinical problems need
the future multi-scale MSK models to be easy-to-use,
robust and also with timely solutions.
It is evident that, for multi-scale modelling of human/animal MSK, from its solution formulation to experimental validation and clinical application, the inherent challenges are hard to be handled based on the
current capacity of experimental and computational
biomechanics. To tackle them effectively, some synergetic efforts are necessary not only by coordinating all
works involved in a coherent way, but also by increasing
and encouraging the level of resources sharing and exchange in biomechanics community, e.g. data and model
sharing (including those developed by commercial
software packages and self-coded models), format
standardization, and dissemination of solution databases
with model distribution.

Acknowledgements
This work was supported by the International
Cooperation Project of National Natural Science

Ren et al.: Biomechanics of Musculoskeletal System and Its Biomimetic Implications: A Review

Foundation of China (No. 50920105504), the UK Engineering and Physical Sciences Research Council Grant
(No. EP/I033602/1), the Project of National Natural
Science Foundation of China (No. 51105167) and the
scientific and technological development planning project of Jilin Province, China (No. 20130522187JH).

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