Computer Methods in Biomechanics and Biomedical

Engineering: Imaging & Visualization

ISSN: 2168-1163 (Print) 2168-1171 (Online) Journal homepage: http://www.tandfonline.com/loi/tciv20

Exploring 3D-structure analysis tools for a

simulated bone remodelling process
A. Ricordeau & N. Mellouli
To cite this article: A. Ricordeau & N. Mellouli (2015): Exploring 3D-structure analysis tools for
a simulated bone remodelling process, Computer Methods in Biomechanics and Biomedical
Engineering: Imaging & Visualization, DOI: 10.1080/21681163.2014.999289
To link to this article: http://dx.doi.org/10.1080/21681163.2014.999289

Published online: 14 Jan 2015.

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Computer Methods in Biomechanics and Biomedical Engineering: Imaging & Visualization, 2015
http://dx.doi.org/10.1080/21681163.2014.999289

Exploring 3D-structure analysis tools for a simulated bone remodelling process

A. Ricordeaua* and N. Melloulia,b
a

Laboratoire MAP5, UMR CNRS 8145, Universite Paris Descartes, Paris, France; bLaboratoire LIASD, EA 4383, IUT de Montreuil,
Universite Paris 8, Saint-Denis, France
(Received 5 February 2014; accepted 13 December 2014)

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The trabecular bone is a complex random network of interconnected rods and plates. Its trabecular structure is constantly
remodelling to ensure a maintenance function. A simulated bone remodelling process was discussed in a previous study
based on a BMU germ-grain model where type and orientation of local structure related to mechanical stress were not
considered. In this study, we explore the potential ability of a 3D-skeleton coupled with a statistical tensor analysis to locally
describe the trabecular structure for binary images. In order to add new constraints for BMU validation and BMU-shape
characterisation in the simulator, we propose a strategy using inertia tensors based on the skeleton ensuring the feasibility of
the entire process.
Keywords: bone remodelling process; simulation; 3D-skeleton; inertia tensor

1. Introduction
The trabecular bone is a porous tissue, which is a network
of interconnected rods and plates. This type of bone is a
highly anisotropic structure that adapts to main direction
stress. Regarding trabecular bone, remodelling has three
functions (Parfitt 2002). First, a maintenance function to
repair fatigue damage which occurs during normal
activity. In response to mechanical stress induced by
external strains, microdamage appears as linear microcracks and diffuse damage. Second, a resistance function:
formation of new bone as a reaction to mechanical stress.
Third, remodelling has a metabolic function to maintain
calcium homeostasis by promoting calcium exchange on
the bone surface (Parfitt 1993). Trabecular remodelling
activity takes place in compact surface saucer-shaped
areas known as bone multicellular units (BMUs). The
BMU remodelling process consists of three main
successive phases, which are activation, resorption and
formation. Activation involves recruitment of osteoclast
precursors and their fusion into osteoclast cells. Following
activation, the resorption phase is carried out by these
osteoclasts that attach and progress on the surface.
Formation is handled by osteoblasts which deposit osteoid
and mineralise it, thus actually forming new bone. Certain
osteoblasts are encapsulated in the osteoid matrix and
transform into cells known as osteocytes, while remaining
osteoblasts continue to synthesise bone until they
eventually transform into quiescent lining cells that
cover the newly formed bone surface. The BMU
remodelling process is thought to have targeted and nontargeted components which were summarised by Burr
(2002) and (Parfitt (2002) as follows. A portion of the

*Corresponding author. Email: a.ricordeau@iut.univ-paris8.fr

q 2015 Taylor & Francis

remodelling process aims at replacing fatigue-microdamaged bone resulting from mechanical stress. Initiation of
such damage repair is dependent upon osteocyte cells
encapsuled in the bone matrix known to act as mechanical
sensors through a network which may be damaged locally
as a result of mechanical stress. However, a substantial
portion (approx. 70%) of the entire remodelling process
does not target this specific purpose. Certain BMUs could
be targeted for removing more fragile hyper-mineralised
bone and serve as fatigue prevention while simultaneously
providing calcium. Initially targeted BMUs could continue
to progress beyond their target. Finally, the origination of
some BMUs could be a non-targeted stochastic process.
The two last mechanisms could result from the influence
of systemic agents such as estrogen and thyroid hormones.
There are currently many remodelling simulation
models which essentially focus on mechanical influence
by using finite-element (FE) methods that measure (SED)
(Hambli et al. 2011, 2013; Marinozzi et al. 2014; Hambli
2014b). Some of these remodelling processes focus
exclusively on structure adaptive change (Wang et al.
2012; Hambli 2014a). Other models integrate microdamage remodelling by taking osteocyte potential for local
remodelling initiation into account. Osteocyte cells which
are encapsulated in the bone matrix are known to act as
mechanical sensors (Robling et al. 2006; Hambli and
Rieger 2011; Rieger et al. 2011). One of the reference
model discussed in Ruimerman et al. (2005) includes
osteocytes. In this model, SED is used to drive a BMUlevel remodelling process where osteoclast and osteoblast
activities are coupled. Locations for osteoclasts to be
activated are chosen randomly on the trabecular bone

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A. Ricordeau and N. Mellouli

surface and restricted to sites expressing a local activation

signal up to a given threshold. Since the activation signal is
calculated as the accumulation of stress energy for
surrounding osteocytes, a high signal can reveal the
presence of damage. Different variations based on this
model were proposed (McNamara and Prendergast 2007;
Van Oers et al. 2010; Wang et al. 2011). Although these
studies are relevant, their limitations can be emphasised.
SED-FE models provide accurate continuous models and
their computation requires calculating many parameters on
a high number of elements at each iteration. Moreover, the
shape of a BMU and the osteoclast progression on the
surface are not clearly defined. For these reasons, it is
worthwhile to conduct stochastic simulations inspired by
SED models. Structural information, local type of bone
(plate or rod) and orientation can be taken into account.
Since recent research on microdamage focused on its
locations and the influence of local trabecular microstructure (Shi et al. 2010), this approach can be adopted.
Various recent works focused on local structure
characterisation for plate and rod voxel-classification in
trabecular bone (Almhdie-Imjabbe et al. 2014). For binary
three-dimensional images, a medial axis (MA) skeleton
was used coupled with a digital topological analysis
(DTA) on skeleton voxels (Peyrin et al. 2010). Different
DTA methods were proposed (Saha et al. 2010) providing
a subtle classification of each voxel-skeleton in junction,
curve, surface and other secondary types. It is worth noting
that MA skeleton implementation is complex and requires
choosing many parameters. Moreover, DTA is very
precise but highly sensitive to noise as local evaluations of
Betti numbers are sensitive to the slightest topological
variation. Hence, DTA cannot be envisaged in a boneremodelling simulator which induces the presence of
disturbances. Moreover, DTA is not adapted to provide
orientation information.
Unlike DTA methods, structure tensors are widely
used to characterise orientation. For a binary image,
trabecular bone global anisotropy is commonly evaluated
using the mean intercept length (MIL) method (Whitehouse 1974). The idea of the MIL method is to count the
number of intersections between boundaries of a structure
and families of parallel lines. A parameter measuring the
degree of anisotropy (DA) is then obtained from an
estimation of the MIL fabric tensor. For a grey-level
image, a tensor based on the gradient image is mainly used
to describe the global anisotropy of a structure. Gradient
vectors are known to be normal to the surface. Hence, MIL
and gradient-based approaches quantify anisotropy of
structures boundaries. Measures of structural anisotropy
using such global structure tensors are based on the
eigenvalue analysis of the matrix they correspond to.
Analogies and limitations of such global structure tensors
(GST) to describe trabecular bone structure were presented
in Tabor (2010).

Structure and orientation can also be described locally

using local structure tensors (LST). LST are estimated for
each voxel through its neighbourhood based on the
gradient-intensity image (7I) or directly on the grey-level
image (I). Gradient local tensor T is estimated using a
Gaussian convolution kernel with a standard deviation
parameter s such as T Gs *7I7I t . These tensors were
used in Westin et al. (1997) for segmentation purposes on
bone data obtained with a computer tomography system.
Local gradient tensors were also used in Moreno et al.
(2011) to estimate a degree of membership in each
structure class for every voxel. This soft classification
was used for estimating global parameters of trabecular
bone for each different structure class. In Vasilic et al.
(2009), a continuous classification of every trabeculae
voxel into rod-like and plate-like structures was
implemented using local inertia tensors directly on the
image intensity rather than on its gradient. Inertia tensors
were calculated for each voxel within a ball neighbourhood with a r radius.
In our previous study (Mellouli and Ricordeau 2011),
we presented a stochastic process for simulating trabecular
bone surface remodelling. The simulated process which
was proposed is an iterative stochastic germ-grain model,
a BMU-level model where each germ corresponds to a
BMU origination and grain to the BMU resorption shape.
Driven by a limited number of parameters which can be
compared to those measuring BMU activity, such as
activation frequency and bone imbalance, this model can
be considered a black-box model. Moreover, it is worth
noting that one of the parameters was proposed to adjust
the degree of priority required for renewing old bone. The
process can therefore be adjusted locally with regard to the
mineral matrix state. This simulator presents certain
analogies with the FE-based models presented earlier,
even though biomechanical processes involved are only
implicitly taking into consideration. Our remodelling
process should incorporate local structure information
(type of local structure and orientation). Such information
can be used to propose BMU shape and direction.
Moreover, new rules for BMU location validation could
be defined. Among the methods presented for this
purpose, it is worth noting that LST-based methods have
the drawback of requiring a s or r parameter, whose
adjustment is dependent upon trabecular thickness.
Furthermore, skeletons have the advantage of being one
voxel thick independently of the structures width. In a
context where global bone structure presents a specific
orientation, our choice in this study was to explore a
simple skeleton version coupled with local inertia tensors
calculated for skeleton voxels only. Such a choice was
motivated by the fact that skeleton and local tensors are
calculated at each iteration of the process. Note that
other existing 3D-skeletons would be worth investigating.
However, this is not the current studys main purpose.

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Table 1.

Skyscan-1072 parameters.

Volume

nx ny nz Age BV=TV BS=TV SMI

V A V plate
V B V rod

3582 499
4082 408

86
64

34
13

9.5
22

DA

0.02 2.18
1.18 1.43

In the following sections, methods are presented and

their feasibility tested by applying the simulator on real
bone samples. Further research should focus on determining values for the simulator drivers which are systemic
parameters and defining local-structure-based rules used
for BMU characterisation. For this purpose, different
simulated evolutions could be proposed and their
relevance evaluated through standard descriptors, such as
Euler number and structure model index (SMI), and
anisotropy measured with the MIL method. Such work
will be necessary to highlight the potential relevance of
this simulator.

2.

Materiel and methods

2.1 Actual volumes

Six volume samples were provided by the IPROS-I3MTO
laboratory at Orleans hospital1 (France). These samples
correspond to femoral head cylindrical biopsies oriented
towards the main anatomical direction. Three-dimensional
binary images were measured with a high-resolution
micro-computed tomography system (Skyscan 1072) with
a resolution of approximately 20 mm. Two volume
samples V A and V B with different porosity and different
structure type were selected for this study. Certain
parameters calculated with Skyscan are presented in
Table 1. Bone volume ratio BV=TV indicates that V A is
twice as dense as V B . Since thickness evaluation by
Skyscan is inversely proportional to BS=BV, V A structures
are thicker than V B structures. The SMI is a structure
parameter which takes values between 0 and 3 (0 for an
ideal plate structure and 3 for an ideal rod structure). The
DA parameter measures the presence of preferential
(a)

Figure 1.

Entire volumes.

direction. In Skyscan-1072 DA values are greater than 1.

This minimum value refers to an isotropic structure.
Parameter values and volume visualisation (Figure 1)
indicate that V A is a dense anisotropic volume composed
with plate-like structure. V B is mainly composed of rods
with different directions. These volumes will be named
V plate and V rod .
Figure 1 displays V plate and V rod which are cylindric
volumes whose principal axis is called the z-axis. This axis
corresponds to the bones main anatomical direction.
Orthogonal slices are called z-slices. V plate is mainly
composed of long plate structures aligned in direction z.
Although both volumes were taken from the same bone
site with an identical protocol, structures in V rod are
markedly different. V rod is mainly composed of rods and
perforated thin plates. However, small plates in direction z
were observed. For both volumes, presence of plates in
direction z is displayed in Figure 2 via dark areas obtained
from the sum of z-slices.

2.2 BMU remodelling model

Remodelling is simulated as an iterative process where
BMUs are principal objects (a BMU level model). Our aim
has been to propose a random description for number,
location and shape of such objects driven with a few
parameters matching classic biological ones as much as
possible. Let us recall that the main parameters commonly
used to describe the biological remodelling process are
activation frequency (AF), related to number of BMUs
activated by unit of time, and balance between formation
and resorption known as bone balance (DB), where a
negative bone balance corresponds to bone loss as
observed in osteoporosis. With BMU shapes corresponding to saucer-shaped cavities resorbed by osteoclasts, DB
represents the lack of volume reformed with new bone.
To measure BMU activity in trabecular bone, the
following formulae have been proposed (Hernandez
et al. 1999) to describe the relationship between AF,
origination frequency (OF), total bone surface area (jSj)
(b)

Vplate

Vrod

A. Ricordeau and N. Mellouli

(a)

(b)

Vplate

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Figure 2.

Vrod

Sum of 50 z-slices (slices perpendicular to the z-axis).

and number (N) of BMUs created per unit of surface and

per unit of time (with W the mean width of BMUs, R the
mean rate of progression across the surface S and s the
mean lifespan of BMUs):
N

AF
jSj
OF
jSj
s:
W
R

At each iteration, a stochastic process is used to simulate

BMU locations with N points or germs taking place
randomly on the surface S, hence a set of random locations
fX 1 ; . . . ; X N }. As the number of BMU is proportional to
jSj, it can be expressed as realisations of a Poisson
distribution with intensity l, thus with mean ljSj. With a
point (germ) X i considered as a BMU origination site and
1i its shape (grain), this can be formulated as a germ-grain
model:

towards highly mineralised bone. Hence, tk is estimated at

distribution
each iteration from an estimated version of M
(f M
) such as:

1 , tk k:
PMx;
Following, the process is summarised through its
algorithm. Let us specify that 1 corresponds to the BMU
grain, hence the resorbed object as can be seen in Figure 3.
For each BMU, 1 f corresponds to the reformed object.
With a the proportion of voxels to be reformed, it results
that j1 f j aj1j. Obviously, when a perforation occurs, no
formation can follow. Figure 4 illustrates different BMU
resorption configurations. Disconnected components
which could result from perforations will be deleted at
each step of the simulator.

<X i % 1i :
However, locations for germs cannot be chosen purely
randomly, meaning uniformly on S. As previously
mentioned, osteocytes encapsulated in the bone matrix
and lining surface cells play a prevalent role in the
biological process. Their signal or lack of signal is likely to
ensure that surface areas which have just been remodelled
are not of primary importance. To this purpose, an
activation energy is calculated at a BMU level. We note
Mx; 1 the state of the mineralised bone matrix for a given
BMU. It is a set of voxel values simply expressed as the
age from last formation. For each new proposed BMU,
validation is acted when average of age voxels in the grain
1 is up a threshold depending on a parameter k:

1 . tk :
Mx;
This threshold tk corresponds to the percentile estimated
for a percentage k. Taken as a global parameter k is thus
related to the fact that the process is more or less targeted

Figure 3. BMU random shape: 1 grain seen in green.

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Computer Methods in Biomechanics and Biomedical Engineering: Imaging & Visualization

Figure 4. Example of resorption formation activity: resorption

in grey (1) and formation in red (1 f ). Shapes without red
correspond to perforations. In (A): disconnections resulting from
resorption. In (B) isolated piece of bone.

Finally, this process is driven with three global parameters

l, a and k related to biological ones. Intensity parameter l

Figure 5.

is related to the activation frequency, hence to the number

of BMUs originated at each iteration. Proportion a of
pixels to be resorbed is related to the bone imbalance,
hence the lifespan and number of osteoblasts. Percentage
k is related to the fact that the process is more or less
targeted as previously defined. Known biological
scenarios can inspire parameters choice. For a normal
bone turnover, corresponding to young healthy bone, the
remodelling process is strongly targeted and the amount
of bone formed equals the amount which was first
resorbed. Such a normal process can be simulated using
a 100% and a high threshold corresponding to
k 90%. Estrogen deficiency after menopause is
known to increase the remodelling rate (higher value
for l). A negative imbalance (a , 100%) with a net
excess of resorption probably due to a prolonged lifespan
for osteoclasts and a reduced lifespan for osteoblasts, is
also observed. Furthermore, failure of the targeting
process may occur when the number of viable osteocytes
decreases due to a system altered by age, a disease such
as osteoporosis or drugs. A threshold more permissive,
choosing k 40% for example, can be used.
2.3 Inertia tensor on a simple skeleton
In a context where global bone structure presents a specific
orientation, we choose to explore a simple skeleton
version coupled with local inertia tensors calculated for
skeleton voxels only. Let us reiterate that this choice is
motivated by the fact that skeleton and local tensors will
be calculated at each iteration of the simulation process.
A simple 3D-skeleton using z-direction (Skz ) is
proposed as follows: the union of 2D-skeletons obtained
from z-slices. Each 2D-skeleton is the result of a thinning
process preserving connectivity and end points. 2D-endpoints are important to preserve in order to keep the most
3D-structure continuity possible. It results that aligned
plates and rods in z-direction are well summarised by Skz
skeleton, represented by a planar surface and a curve,
respectively. Skz can capture structure elements for which
the orientation varies gradually from z-direction to an
orthogonal direction. Gradual changes of structure orientation are correctly detected. However, a perpendicular

Skz visualisation for sub-volumes composed of 50 z-slices, V rod (top) and V plate (bottom).

A. Ricordeau and N. Mellouli

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Figure 6. Visualisation of inertia tensors p

T
using ellipsoids having eigenvectors ui as principal axes. u1 in blue, u2 in green and u3 in red.
Each vector has a norm equals that to 2:5 li .

curvature induces missing voxels. Skeletons are visualised

in Figure 5 for sub-volumes V rod and V plate composed of
50 slices. Skz is simple but seems well suited to these
volumes. Skz has the advantage of being easy calculated.
Inertia tensor TP at voxel P is the covariance matrix
associated to positions of voxels which are present in a
neighbourhood N P. Hence, TP is a symmetric positive
second-order tensor that can be decomposed according to
the spectral theorem. With each li eigenvalue associated
to eigenvector ui , this yields:
TP VarN P l1 u1 ut1 l2 u2 ut2 l3 u3 ut3 :
Visualisation of TP can be made using an ellipsoid
having eigenvectors as principal axes as seen in Figure 6,
with conditions on sorted eigenvalues (0 # l3 # l2 # l1 )
being related to the different neighbourhood shapes as
summarised in Table 2.
Another useful decomposition of T in a tensor base
allows a direct interpretation of its positive coordinates in
terms of the three local structure shapes:
T l1 2 l2 T 1 l2 2 l3 T 2 l3 T 3 :
Hence, positive coordinates divided by l1 can be seen as
certainty for T representing a linear (mL ), a planar (mP ) or
an isotropic structure (mI ). For inertia tensors calculated
using Skz skeleton, associated membership functions can
be visualised in Figure 7. Moreover, as their sum
(mL mP mI 1), these membership functions can be
used for a classification purpose, where each voxel Pi is

Table 2.

Eigenvalue conditions

Linear (L)
Planar (P)
Isotropic (I)

0 l3 l2 p l1
0 l3 p l2 l1
0 , l3 l2 l1

P [ Skz ! N P [ dSkz > V:

2.4

Local BMU characterisation

Let us reiterate that the aim of this tensor-skeleton

exploration is to integrate local structure information in
our simulated process. In our algorithm, BMU validation
and BMU shape choice should integrate such information.
For each BMU candidate located at a surface voxel x, we
propose to evaluate local information from nearby
skeleton voxels only. A Lx set of skeleton voxels can be
obtained using geodesic propagation in the volume from x
to the skeleton. When the first skeleton voxels are attained,
propagation is extended a few steps further to obtain the Lx
set of skeleton voxels for which tensors will be calculated
as previously presented.
x [ surface ! Lx fPi [ Skz };

Ideal eigenvalue conditions.

Class

assigned to the class C i [ fL; P; I} having the maximum

membership function: mi maxfmL ; mP ; mI }. Labels
obtained from inertia tensor calculated for each skeleton
voxel are visualised in Figure 8 for our two volumes. It is
important to specify that the neighbourhood N P is
obtained by a propagation in the intersection between a
dilated skeleton Skz and the volume V. A unique isotropic
morphological dilatation is used to densify the neighbourhood, which permits avoiding classification errors in flat
areas where voxels are missing. It also improves
classification of interconnection areas. For each skeleton
voxel, the propagation was done with a distance equal to 3
to obtain a neighbourhood as previously described:

Structure

Pi [ Lx ! N Pi [ dSkz > V ! TPi :

Rod or edge
Plate
Junction

Figure 9 illustrates this local relationship between surface

x voxels and Lx , which avoids expensive tensor
evaluation for all skeleton voxels at each iteration of

Computer Methods in Biomechanics and Biomedical Engineering: Imaging & Visualization

0.8

(a)

0.8

(b)

0.7

0.7

0.7

(c)

0.6

0.6

0.6

0.5
0.5

0.5

0.4
0.4

0.4

0.3

0.3
0.3
0.2

0.2

0.1

0.1

0.2
0.1

mL =

12

mP =

23

mI =

3
1

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Figure 7. Visualisation on a 3D-skeleton of the three membership functions. From left to right: mL , mP and mI . Comprised between 0
and 1, their values are coloured from dark blue to dark red.
(a)

(b)

Vrod

Figure 8.

Vplate

Hard classification visualisation: blue for L, green for P and red for I.

Figure 9. Relation between surface voxel x (black voxel) and skeleton voxel set (Lx ) with hard classification and associated direction for
involved skeleton voxels. Smoothed Skz in grey, smoothed surface in blue for a neighbourhood of voxel x.

the simulator. Subsequently, decision regarding a BMU

candidate can be implemented using tensor information.
For each skeleton voxel Pi in Lx , membership functions
mL ; mP ; mI and principal directions u1 ; u2 ; u3 are
available, and geodesic distance between surface voxel
x and Pi is also available. Direction for a linear structure
(L) refers to u1 while normal direction for a planar
structure (P) refers to u3 . When mL is close to mP , a strict
classification is not reliable, particularly when directional
information is required. This situation illustrated in

Figure 10 is not exceptional. Information obtained from

voxels in Lx should permit us to determine different
decision rules for the simulator. For example, we can
require that damage is more likely to appear on rods in a
given direction related to an external stress force.
Moreover, a BMU shape may be conditioned by
information related to certain voxels in Lx .
By removing ambiguously classified voxels, decision
rules can be based on reliable voxels only to avoid false
interpretation to the greatest extent possible.

A. Ricordeau and N. Mellouli

1
0.9
0.8
0.7
m(planar)

0.6
0.5
0.4
0.3
0.2
0.1

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0.2

0.4

0.6

0.8

m(linear)

Figure 10. An example of membership functions mL ; mP values. Colours are corresponding to hard classification: blue for linear, green
for planar and red for junctions.

function of the three Betti numbers (x b0 2 b1 b2 )

where b0 is the number of separate bone component, b1 is
the number of handles (number of redundant connections)
and b2 the number of enclosed cavities (Odgaard and
Gundersen 1993). The surface bone remodelling process

3. Results
First, the simulator was implemented in different contexts
using the actual selected volumes. Volume evolution is
monitored by the relative-volume parameter and the Euler
number (x) which is a connectivity parameter. x is a

500

500

1,000

1,000

1,500

1,500

2,000
2,000
2,500
0

10

12

10

12

10

12

1
0.9

0.9

0.8
0.8
0.7
0.7

0.6
0

6
Vplate

10

12

Vrod

Figure 11. For entire volumes: evolution of parameters in function of the iteration number (k). Euler number (top) and relative volume
(V k =V 0 ) (bottom). Blue curves for the targeted process (a 50%, k 85%) and red curves for the less targeted process (a 50%,
k 40%).

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Computer Methods in Biomechanics and Biomedical Engineering: Imaging & Visualization

Figure 12. Evolution using the simulator for V plate (left) and V rod (right). Skz skeleton behaviour and tensor hard voxel-classification
behaviour. Blue lines: directions for linear classified voxels, green smoothed surface for planar classified voxels, red voxels for
intersection classified voxels. Initial sub-volumes (top) and final sub-volumes (bottom).

Downloaded by [Laurentian University] at 02:38 04 April 2016

10

A. Ricordeau and N. Mellouli

ensures that enclosed cavities do not occur, thus:

x b0 2 b1 . Upon initialisation, trabecular bone has
one connected component (x 1 2 b1 ).
Two scenarios based on global parameters are now
presented, both having negative imbalance with a proportion
of voxels to be reformed (a being less than 1). We reiterate
that high values for parameter k pertain the fact that the
process is targeted towards highly mineralised bone.
Therefore, the first scenario is called the targeted scenario:
(l 5%, a 50%, k 85%) and the second the
untargeted scenario: (l 5%, a 50%, k 40%).
Figure 11 displays evolution curves of the Euler
number for the two scenarios and volumes. Upon
initialisation: b1 300 for V plate and b1 900 for V rod .
These values correspond to the number of tunnels or
handles in each connected structure. One perforation in the
structure induces an increase of 1 for b1 ; one cut of the
structure induces a decrease of 1 for b1 . For the untargeted
process, a decrease of x can be explained by an increase in
the number of perforations. This result is observed for both
volumes. For V plate , values of x are nearly constant
regarding the targeted process. With this scenario, there is
no modification of connectivity during a decrease in
volume. In this case, the targeted scenario with a 50%
can be regarded as a thinning process.
Second, simulations without formation were
implemented with a 0% to test both Skz skeleton
behaviour and tensor voxel-classification behaviour during
this artificial extreme evolution. It is worth noting that in
such a context, parameter k is not relevant since voxel-age
is simply referring to the process iteration number. Since
surface is only subject to random local resorption, surface
gradually becomes a rugged landscape during the process.
When thin plate and rod structure perforations occur, small
pieces of bone may disconnect. As such small connected
components are removed during the process, rods may
partially disappear and thin plate large perforations may
occur. The skeleton is impacted by surface roughness, thus
a pruning stage will be added at each iteration to remove
induced pics to the greatest extent possible. Pruning is
important but cannot be implemented completely. In any
event, the impact of small imperfections (e.g.: small pics
remaining on the skeleton) is not essential for inertia
tensor calculation. Each tensor TP is a covariance matrix
whose eigenvectors give principal directions, as used in
principal component analysis (PCA), based on all a
neighbourhood N P. Such a statistical method is more
robust than a strict topological analysis (DTA methods).
Visualisations with this extreme scenario are presented
in Figure 12 for V rod and V plate sub-volumes. For V plate
which is a volume composed of thick plates oriented in zdirection, plates are thinning and thinner plates are
perforated. It is worth noting that junction components
(red voxels) present a certain stability both in shape and
direction. When such components are associated to plate

interconnecting in direction z, they have linear shapes.

This information could be used to construct a parameter
which determines the presence and orientation of
intersecting plates. For the thin V rod volume, interpretation
of such junction components may not be possible
specifically for an evolution of the simulated process in
such an extreme scenario. Surface roughness induces false
interpretation of junction components which are more
likely to be displayed as noisy small components.
4.

Conclusion

The simulated process which was proposed is an iterative

stochastic germ-grain model driven by a limited number of
global parameters. Similar to the biological remodelling
process, it is a BMU model where germ corresponds to
BMU origination and grain corresponds to BMU
resorption shape. A global constraint based on global
state of the mineralised bone matrix and a local constraint
based on local structure type and orientation are proposed
for validating BMU. A simple skeleton calculated in the
prevalent direction (anatomical direction) is used by a
local tensor to characterise local structure information.
Integrating this local information to the simulator is
discussed. For instance, a simple relationship between a
BMU surface-voxel candidate and a skeleton voxel set is
established for validating BMU. Such a relation avoids
lengthy tensor computation by focusing on local skeleton
voxel set only.
At this stage, all functionalities needed by the
simulator are available. These functionalities are: skeletonisation of the entire volume, inertia tensor for a skeleton
voxel and local relation between a surface voxel x with a
list Lx of skeleton voxels. They were implemented and
tested on two real volume samples. Evidently, some
adjustments must still be implemented.
Expert advice is required to suggest pertinent decision
rules, based on Lx structure and orientation information, to
be used for BMU-shape specification and BMU validation
at x germ location. It is worth noting that BMU shapes and
sizes should be adapted to the various volume structures.
In particular, thin structures require realistic BMU-depth
adjustments. In this perspective, we can quote a recent
study (Goff et al. 2012) which emphasises that size and
location of resorption cavities are influenced by local
structure. These cavities were associated to structure type
(plate, rod and intersection) and minutely measured on 3D
images corresponding to nine vertebral samples. Based on
such a study and expert opinion, new constraints could be
used to validate a BMU candidate in our algorithm.
Moreover, the current study has limited itself to
specific structures with a prevalent direction. In order to
explore a larger data-set of volumes, other skeletons that fit
more complex structures and require short computing
times would be worth investigating.

Computer Methods in Biomechanics and Biomedical Engineering: Imaging & Visualization

Finally, assuming that the skeleton- and BMU-related
parameters are accurately adjusted, different scenarios
based on (l, a, k) simulator parameters can be proposed in
order to follow the evolution of 3D parameters. The
random aspect of this simulator might be relevant for
studying 3D parameter sensitivity.

Acknowledgements
The authors would like to thank Dr Eric Lespessailles and Dr
Claude-Laurent Benhamou from IPROS-I3MTO laboratory in
Orleans (France). We are also grateful to Jerome Touvier for his
invaluable help.

Conflict of interest disclosure statement

Downloaded by [Laurentian University] at 02:38 04 April 2016

No potential conflict of interest was reported by the authors.

Note
1.

http://www.univ-orleans.fr/i3mto

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