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Abstract
Throughout life, bone is continuously turning over by the well-regulated processes of bone formation and resorption. Everyday
activities damage bone, and this damage is normally repaired in a continuous remodelling process. When an imbalance in this
remodelling process occurs, bones may become more susceptible to fracture. This paper is devoted to a theoretical modelling of the
competition between damage and internal remodelling in bones. The general theory of adaptive damaged-elastic materials proposed
here as a model for the physiological process of damaged-bone remodelling follows the general framework of continuum
thermodynamics where new damaged-bone remodelling law and associated thermodynamical restrictions are stated, and specialized
to the case of small strain in isothermal processes. An attempt is also made to derive: (a) the damage force (adaptive damage energy
release rate ) which controls the microcracks propagation and arrest, and (b) the damage rule by introducing damage thresholds and
loading/unloading conditions. # 2001 Elsevier Science Ltd. All rights reserved.
Keywords: Bone adaptation; Damage mechanics; Adaptive energy release rate; Continuum thermodynamics
0021-9290/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 2 1 - 9 2 9 0 ( 0 0 ) 0 0 2 1 5 - 3
472 S. Ramtani, M. Zidi / Journal of Biomechanics 34 (2001) 471–479
Despite the fact that damage accumulation has been cells. Energy and entropy may also be transferred to or
demonstrated in living bone and postulated as a from the matrix structure by these chemical reactions.
stimulus to the bone modelling and remodelling (c) The extracellular fluid is always in contact with the
response, a relationship between microdamage and blood plasma. The plasma supplies the materials
adaptive bone-remodelling was only tentatively pro- necessary for the synthesis of bone matrix. (d) The
posed. Frost (1960) offers the idea that microdamage characteristic time of chemical reaction is several orders
may trigger a remodelling response via the canalicular of magnitude greater than the characteristic time
network surrounding the osteocytes. According to this associated with a complete perfusion of the blood
theory, there is a physiological strain range where bone plasma in the bone, hence any excess of heat generated
is in equilibrium, determined by metabolic factors alone. by the chemical reactions is quickly carried out by the
The lower limit of this range is given by a ‘‘remodelling’’ circulation.
process while the upper limit is given by a ‘‘modelling’’
one. The author suggested that these processes are 2.1. Strain- and damage-induced remodelling
stimulated if the rate of microdamage formation is due
to unphysiological strains. Chamay and Tschantz (1972) From theoretical point of view, it makes sense to
have observed damage in vivo as ‘plastic slip lines’ or consider strain as the basic mechanical signal, because it
collagen bundle ‘wrinkling’ in the area where remodel- is: (a) the immediate local effect of external bone
ling by bone deposition was most extensive. Carter and loading, and (b) a primary and directly measurable
Hayes (1977) have hypothesized that fatigue damage physical quantity (and not the stress which is as well
acts to produce a bone maintenance stimulus. This defined but not directly measurable quantity). Thus,
hypothesis was developed by Prendergast and Taylor Justus and Luft (1970) demonstrated that straining bone
(1994) to predict the time-course of bone adaptation, by will increase the calcium concentration in the interstitial
accounting for the accumulative nature of the damage fluid. They showed that this was due to a change in the
with the concept of a continuous damage rate. Recently, solubility of the hydroxyapatite crystals and also
Prendergast and Huiskes (1996a) have proposed a demonstrated this mechano-chemical effect with inor-
microstructural finite element analysis to explore the ganic crystals in vitro.
relationship between damage formation and local strain As pointed by Huiskes (1997), assuming microcracks
of osteocyte-containing lacunae for various types of development as the stimulus for bone remodelling is
damage. Their study was based on the hypothesis that, if very tempting for a number of reasons: (a) the
the microstructural changes are substantial enough, and continuous physiological process of resorption and
the osteocytes do function as strain sensors then damage deposition makes no sense other than as a repair
would stimulate bone remodelling using the osteocyte- process for microdamage, (b) bone repair is a well-
sensor mechanism. The three microdamage mechanisms known biological phenomenon; any other assumption
tested by the authors are the following: (a) collagen for a stimulus effect requires the introduction of
bundle break-down, which occur when the collagen biological mechanisms of which the actual existence is
fibrils separate from the supporting hydroxyapatite unknown, and (c) the development of microdamage is
crystals, (b) the interlamellar debonding and (c) the automatically related to the dynamic loading history,
microcracking in the cement-line. Their results have which is not the case for the other possibilities
given theoretical support to the experimental studies mentioned above.
that have shown a correlation between microdamage
and the initiation of resorption as the first step in bone 2.2. Kinematics
remodelling.
The motion of material point is described in the
Cartesian system by yi ¼ y~i ðxk ; tÞ where y~i ðxk ; tÞ gives
2. Basic and fundamental assumptions the location of the material particle xk at time t:
14i; k43, i and k are indices labelling the three different
To construct a general framework for a phenomen- coordinate directions in the spatial and reference
ological description of both strain- and damage-induced configurations, respectively. The deformation function
bone remodelling process, we invoke the following yi ¼ y~i ðxk ; tÞ is assumed to be one to one, continuous
assumptions (Cowin and Hegedus, 1976): (a) The and invertible. The velocity field of the continuum at
porosity of the bone matrix is affected by the ambient time t, is given by vi ¼ @yi =@t. The deformation gradient
long-term strain history of the bone, by the addition of Fik , the local volume change J and the velocity gradient
mass or the removal of mass from the bone matrix and Lij are, respectively, defined by
by the presence of the microcracks in the bone matrix. (b)
The transfer of mass occurs as the result of a @yi
Fik ¼ ; ð1aÞ
biochemical reaction which is mediated by the bone @xk
S. Ramtani, M. Zidi / Journal of Biomechanics 34 (2001) 471–479 473
J ¼ det F ð1bÞ may change without changing the reference state for
strain if we assume that, at constant temperature and
and zero body force, there exists a unique zero-strain
@vi reference state for all values of x (Cowin and Hegedus,
Lij ¼ : ð1cÞ 1976). Thus, by combining Eqs. (2) and (3), the bulk
@xj
density r of the damaged porous structure is stated as
For one, we will consider the bulk density r of the gx
damaged porous structure to be expressible as r ¼ ð1 d Þ : ð4Þ
J
r ¼ gf; ð2Þ
where g is the density of the material that composes the
bone matrix and f is the volume fraction of that 3. Field equations
material present (current solid volume fraction). Both f
and g can be considered as field variables by the same We consider an arbitrary fixed surface S enclosing a
arguments as employed in Goodman and Cowin (1972). volume O of the porous matrix structure. Because mass
The internal remodelling variable was initially intro- is being added to the body, the traditional transport
duced by assuming: (a) the bone as a porous elastic theorem has been modified as follows (Cowin and
solid, and (b) the normal adaptive process that occur in Hegedus, 1976; Coussy, 1995):
Z Z
bone remodelling as strain controlled mass deposition D
gfg dO ¼ ðmg þ gfg_ Þ dO; ð5Þ
and resorption processes which modify the porosity of Dt O O
the porous elastic solid. If x denotes the volume fraction where both the derivative indicated and the super-
of the matrix material in an unstrained reference imposed dot are the material or substantial time
configuration, the physical meaning of the variable x is derivatives, g denotes an arbitrary field quantity, and
taken from Cowin and Hegedus (1976) : one might m is the rate at which mass per unit volume is added to
imagine a block of porous elastic material with the four or removed from the porous matrix structure (m arises
points, the vertices of a tetrahedron, marked on the from chemical reactions). If the differentiation indicated
block for the purpose of measuring the strain. When the in Eq. (2) is performed in the case where g is chosen as
porosity changes, material is added or taken away from the identity function (i.e., g ¼ 1) and the result written
the pores, but if the material is deformation-free it as a field equation, we have
remains so and the distance between the four vertices
marked on the block do not change. Thus x can change gf þgfLkk ¼ m ð6Þ
while the zero-strain reference state remains the same.
Secondly, damage can be described as the local loss of which is the local statement of balance of mass for the
mechanical integrity or the ‘state of partial cracking’ due porous matrix.
to nucleation and growth of microcracks (Kachanov, When Eq. (4) is substituted into the statement of mass
1980; Krajcinovic et al., 1987; Krajcinovic and Lemai- balance (6), a new relation between the rate of change of
tre, 1987; Chaboche, 1988, Ramtani et al., 1992). In the remodelling variable x, _ the mass deposition or
most of the studies concerning the development of resorption m and the damage rate d_ is stated as
damage in bone (as measured by a reduction in elastic (Ramtani and Zidi, 1999)
modulus) during the fatigue tests, the damage is
m xd_
represented by a scalar variable d (Zioupos et al., x_ ¼ J þ ; ð7Þ
1996; Prendergast and Huiskes, 1996a). gð 1 d Þ ð 1 d Þ
By analogy with the effective strain or stress concept which can be viewed as an extension of an earlier
(Kachanov, 1958; Chaboche, 1988, Ju, 1989), we proposal (Cowin and Hegedus, 1976) by introducing the
introduce the effective volume fraction of the matrix damage variable.
structure in an unstrained reference state as xd , and by Firstly, note that an increase of the damage level in
the use of the intrinsic incompressibility condition of the the bone material leads to an increase in the remodelling
damaged solid phase (Suh and Spilker, 1994), we have rate, which is in accordance with Prendergast and
xd ¼ ð1 d Þx ¼ Jf: ð3Þ Taylor (1994), and Prendergast and Huiskes (1996a),
who have demonstrated that damage-stimulated resorp-
d
Then, a formal definition of x can be made in terms of tion could be a local manifestation of strain-adaptive
the volume fraction f associated with the strain-state remodelling. Secondly, the proposed remodelling rule
characterized by the local volume change J. In other follows the idea that more than one control system may
words, x and f are the same but viewed from the be operative in bone mass regulation (Carter, 1984). In
effective free deformation reference state and the current particular, it has been suggested that the remodelling
deformed state, respectively. Note that both x and xd stimulus is not exclusively damage or strain but rather
474 S. Ramtani, M. Zidi / Journal of Biomechanics 34 (2001) 471–479
that both operate together in a process of maintaining equivalent to the following two balance equations in
mass and avoiding failure (Prendergast and Huiskes, differential form:
1995). @Tki
From Eq. (7), it becomes clear that the remodelling þ gffi þ pi ¼ gf_vi ; ð11aÞ
@yk
rate can be cast in two terms: (a) the first one is linked to
the elastic opening of the existing (or strain-induced) @Qk
microcracks, and (b) the second is due to the damage gfU_ gfr þ Tki Lik h ¼ 0; ð11bÞ
@yk
growth (coupled term). On the other hand, if we look for
the case where the bone material is submitted to loads which are customary and, respectively, the local version
(or strains) such as no further damage takes place, the of balance of linear momentum for the porous matrix
damage growth do not contribute to the remodelling and the local energy equation for the porous matrix.
process (i.e., d_ 0 and d 1) and leads to
J m
x_ ¼ ð8Þ 4. Second axiom of thermodynamics
ð1 dÞ g
which is similar to the one obtained by Cowin and Consider an entropy production inequality of the
Hegedus (1976) with d ¼ 0 and corresponds probably to form (Coleman and Gurtin, 1967; Malvern, 1969;
the case where the bone turnover rate is sufficient to Germain, 1973; Bowen, 1976; Cowin and Hegedus,
mend the microdamage as it is formed. In order to show 1976)
Z Z Z
that there exist situations where bone fractures are never D r Q k nk
repaired, let us investigate the singular case where d_ 6¼ 0 gfZ dO5 gf dO dS
Dt O O y @O y
and d 1. When imposed on Eq. (7), the following Z !
remodelling rate is obtained by x_ !/, and this yielding h~
þ þ Zm dO; ð12Þ
to infinity is incompatible with the well-known fact that O y
the time scale of the remodelling processes is of the order
where the scalar Z is the specific entropy, y is the local
of months or possibly years.
temperature and h~ is defined in the same fashion as h
The system to which Eqs. (9) and (10) apply is the
above. The distinction between h and h~ is made to
porous matrix structure while the effect of the internal
indicate that all the energy transferred from the
perfusant is accounted for by transfer terms in each
perfusant to the matrix need not contribute to the
equation. We postulate, respectively, a balance of
entropy production. By a known standard argument
momentum and a balance of energy at time t in the
(Coleman and Noll, 1963), the local form of the entropy
form (Coleman and Gurtin, 1967; Malvern, 1969;
inequality is
Germain, 1973; Bowen, 1976 ; Cowin and Hegedus,
Qk @y
1976) gf Zy_ þ C þ Tki Lik þ h * 50; ð13Þ
Z Z Z y @yk
D
gfvi dO ¼ Tij nj dS þ gffi dO
Dt O @O O where h * ¼ h h~ and C ¼ U Zy is the Helmholtz free
Z
energy density. However, there are several other
þ ðpi þ mvi Þ dO; ð9Þ specialized approaches that leads to the same results
O
Z Z (Cowin, 1999).
D 1
gf vi vi þ U dO ¼ gfðr þ fi vi Þ dO
Dt O 2 O
Z
5. Constitutive assumptions and thermodynamical
þ ðnk Tki vi ni Qi Þ dS restrictions
Z@O
1
þ pi vi þ m vi vi þ U þ h dO; ð10Þ A thermodynamic process for the composite bone
O 2
material under discussion is a set of scalar functions
where vi , Tki , fi , U, r and Qi are respectively an (Coleman and Gurtin, 1967; Germain, 1973; Bowen,
arbitrary velocity field of the continuum at time t, 1976; Cowin and Hegedus, 1976) from which the free
the Cauchy stress tensor, the specific body force, the energy is chosen as (Miehe, 1995)
specific internal energy, the specific heat supply function ~ ðy; Fik ; xÞ:
C ¼ ð1 d ÞC ð14Þ
per unit time and the heat flux vector. Besides, pi is the
force the perfusant applies to the porous matrix Taking the time derivative of the free energy
structure and h represent any energy transfer due to function (14), substituting into (13), and making use of
the local interaction between the matrix and the standard arguments (Coleman and Gurtin, 1967;
perfusant. Under suitable smoothness assumptions the Germain, 1973; Bowen, 1976; Cowin and Hegedus,
balance equations (9) and (10) in integral form are 1976), we obtain the following restrictions which
S. Ramtani, M. Zidi / Journal of Biomechanics 34 (2001) 471–479 475
corresponds to the caloric equation and the behavior al., 1987; Chaboche, 1988; Prendergast and Taylor,
law for the damaged bone: 1994), or derived directly by means of damage criterion,
@C damage consistency condition and loading/unloading
Z¼ ; ð15aÞ conditions (Chaboche, 1988; Ju, 1989, Ramtani et al.,
@y
~ 1992).
gx @ C Eqs. (1a), (3), (7), (15b) and (19) and the damage
Tij ¼ ð1 d Þ2 Fjk : ð15bÞ
J @Fik evolution law (to be specified) can be viewed as a system
From the fundamental assumptions, we have supposed of 21 scalar equations for the 21 scalar unknowns Tij ,
that, at constant temperature and zero body force, there Fik , y~i , r, x and d.
exists a unique zero-strain reference state for all values
of x which can now be written as
7. Small-strain approximation
Tij ðy0 ; dik ; x; d Þ ¼ 0; ð16Þ
where y0 and x are, respectively, the fixed temperature To set the stage for the small-strain approximation,
and an arbitrary value of the remodelling variable. the independent variables x and Fik are changed to e and
By substituting Eq. (15) back into Eq. (13) and Eij where e is a measure of the change in volume fraction
making use of Coleman and Noll (1963) arguments, from a reference volume fraction x0 (Hegedus and
the reduced entropy inequality becomes Cowin, 1976),
~
@C Qk @y e ¼ x x0 : ð22Þ
x ð1 d Þm þ h * 50 ð17Þ
@x y @yk The new functions are now denoted by superposed bars,
and
e; Eij ; d ¼ m
m ~ ðx; Fik ; d Þ; ð23aÞ
~
gx @C ~ _
ð1 d Þ x C d50 ð18Þ e; Eij ¼ C
C ~ ðx; Fik Þ; ð23bÞ
J @x
Note that the entropy inequality (17) has been stated by where the linearized strain tensor E has the following
Cowin and Hegedus (1976) for the ‘‘undamaged’’ bone representation in terms of displacement gradient
material and that (18), can be viewed as a new
Eij ¼ 12 ui;j þ uj;i : ð24Þ
thermodynamical restriction for the damage dissipation
of the adaptive-elastic bone material. The constitutive equation for the stress takes the form
2 g ð x0 þ e Þ @C
sij ¼ ð1 d Þ Fik Fjl ð25Þ
½detð1 þ 2EÞ
1=2 @Ekl
6. A summary of the theory
and Eq. (7) can be reduced as
We now summarize the equations that constitute the 1 n
o
proposed theory in the quasi-static and isothermal e_ ¼ F e; Eij ; d þ ðx0 þ eÞd_ ; ð26Þ
ð1 d Þ
processes. These equations are the deformation gradient
given by Eq. (1a), balance of mass in the form (7), the where
balance of linear momentum (11a) as e; Eij ; d ¼ 1m
F e; Eij ; d ½detð1 þ 2EÞ
1=2 : ð27Þ
@ski g
þ gffi ¼ 0; ð19Þ
@yk Based on substantial physical justification (Scott, 1957;
where the inertia term (quasi-static assumption) and the
Bonfield and Li,
1966),
the approximations for F
perfusant force pi have been neglected, the volume
e; Eij ; d and C e; Eij are obtained by neglecting the
fraction of the reference configuration x defined by terms of order 3 in a Taylor series expansion,
Eq. (3), the behavior law (15b). The quantities m and C ðe; Eik ; d Þ ffi aðe; d Þ þ Aij ðe; d ÞEij
F
are functions of Fik ; x and d,
þ 12Bijkm ðe; d ÞEij Ekm ; ð28aÞ
m¼m
~ ðFik ; x; d Þ; ð20aÞ
~ ðFik ; xÞ; C ðe; 0Þ þ 1 Cijkm ðeÞEij Ekm ;
ðe; Eik Þ ffi C ð28bÞ
C ¼ ð1 d ÞC ð20bÞ 2g
~ ðFik ; xÞ satisfy the condition
and it is required that C where
@C~
ðe; 0; d Þ;
aðe; d Þ ¼ F ð29aÞ
dij ; x ¼ 0; ð21Þ
@Fik
@F
and the damage evolution law which can be evaluated Aij ðe; d Þ ¼ ðe; 0; d Þ; ð29bÞ
by the use of the remaining life approach (Krajcinovic et @Eij
476 S. Ramtani, M. Zidi / Journal of Biomechanics 34 (2001) 471–479
unloading conditions. For convenience, we define the As a summary, the basic system of equations for the
notation as proposed theory consist of the equilibrium equation (19)
ðe; Eik Þ:
Y * ¼ jY j ¼ C ð39Þ where, to terms of first order in strain, the bulk density r
given by (4) is rewritten as
The state of damage in the material is
then characterized
by means of damage criterion ‘ Yt* ; kt with the r ¼ ð1 d Þgðx0 þ eÞð1 Ekk Þ; ð45Þ
following functional form:
the stress–strain relation (30), the remodelling rate
‘ Yt* ; kt Yt* kt 40; t 2 Rþ : ð40Þ
equation (31), the strain-displacement relations (24)
Here, the subscript t refers to the value at current time, and the damage rate equation (41). This is a system of 17
and kt signifies damage threshold (energy barrier) at scalar equations involving the 17 scalar unknowns, Tij ,
current time t (i.e. the radius of the damage surface). If Eij , ui , e and d.
k0 denotes the initial damage threshold before any
loading is applied, condition (40) then states that
damage in the material is initiated when the damage
9. Conclusion
energy release rate Yt* exceeds the initial damage
threshold k0 . Note that the above energy-based damage
From biomechanical point of view, there is a
criterion is fundamentally linked to the history of the
great need that an attempt be made to put some
bone’s loading.
framework in which theoretical statement can be
Furthermore, initial microdamage can (i) also pre-
made about the damage effect on the bone adaptation
exist even if the bone material is free deformation, (ii)
process. To achieve this goal, we have used continuum
participate in the remodelling process as an elastic
thermodynamics and stated some new results which
opening, and (iii) can propagate only if the new damage
can be viewed as: (a) an extension of the theory of
threshold is reached. To describe the damage growth
adaptive elasticity, presented by Cowin and colleagues
and the expansion of damage surfaces, it is necessary to
(Cowin and Hegedus, 1976; Hegedus and Cowin,
specify the equations of evolution for d and k. In order
1976), by introducing the presence of the microcracks,
to describe the microdamage (microcrack) growth
(b) and as a logical following of the mathematical
without considering the microcracks interactions, we
model proposed by Prendergast and Taylor (1994).
define the general evolution rule as (Chaboche, 1988; Ju,
The essential purpose of the present work is to
1989; Ramtani et al., 1992; Miehe, 1995)
demonstrate one possible way for modelling the
d_ ¼ lH
_ Yt* ; dt ; k0 k_t ¼ l;_ ð41Þ damage interaction with remodelling process in bones
_
where l50 is a damage consistency parameter which and we can summarize the main points of this work as
defines damage loading/unloading conditions according follows:
to the Kuhn–Tucker relations: 1. The proposed remodelling rule follows the idea
that: (a) more than one control system may be operative
_
l50; ð42aÞ in bone mass regulation (Carter, 1984), (b) the
remodelling stimulus is not exclusively damage or strain
‘ Yt* ; kt 40; ð42bÞ
but rather that both operate together in a process of
maintaining mass and avoiding failure (Prendergast and
_ Yt* ; kt ¼ 0:
l‘ ð42cÞ
Huiskes, 1995). From this study, it becomes clear that
In order to derive the damage consistency
parameter,
let the remodelling rate can be cast in two terms where the
us consider two possible events: (a) if ‘ Yt* ; kt 40, the first one is associated with the elastic opening of the
damage criterion is not satisfied and by condition (42c) existing microcracks, and the second is due to the
we have l_ ¼ 0; hence, the damage rule (41) implies that damage growth. Besides, the associated state laws and
d_ ¼ 0 and no further damage takes place, (b) if l50, _
thermodynamical restrictions (dissipative inequalities)
that is further damage
is taking place, condition (42c) are also stated for the general theory.
now implies that ‘ Yt* ; kt ¼ 0. In this event the value of 2. We have investigated, by the use of an approxima-
_
l50 is determined by the ‘‘damage consistency con- tion scheme involving series expansion, the possible
dition’’; i.e. small-strain formulation of damaged-bone remodelling
‘ Yt* ; kt ¼ ‘_ Yt* ; kt ¼ 0 ð43aÞ theory. In particular, we have derived the basic system
of governing equations and identified, under some
) l_ ¼ Y_ t* : ð43bÞ suitable assumptions, the damage force for driving the
So that kt is given by the expression damage evolution. In particular, the new concept of
adaptive damage energy release rate is introduced. The
kt ¼ max k0 ; max Ys : * ð44Þ local damage initiation and propagation are linked to
s2½1;t
the damage force, which is checked against the debond-
478 S. Ramtani, M. Zidi / Journal of Biomechanics 34 (2001) 471–479
ing energy (current damage threshold) required for Cowin, S.C., Hegedus, D.M., 1976. Bone remodelling I: theory of
microcrack growth. adaptive elasticity. Journal of Elasticity. 6, 313–325.
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standing and quantitative description of the functional induced by a medullary pin. Journal of Biomechanics 11, 269–275.
Frost, H.M., 1960. Presence of microscopic cracks in vivo in bone.
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Bulletin of Henry ford Hospital 8, 25–35.
tion of that functional adaptation. The process to be Germain, P., 1973. Cours de mécanique des milieux continus. Masson,
followed to achieve these goals will involve a combina- Paris.
tion of this theory, experiments (Scott,1957; Bonfield Goodman, M.A., Cowin, S.C., 1972. A continuum theory for granular
and Li,, 1966), stability analysis (Zidi and Ramtani, materials. Archieve Rational Mechanics and Analysis 44, 249–266.
1999) and numerical implementation of the proposed Hart, R.T., Davy, D.T., Heiple, K.G., 1984. A computational method
model in finite element code (Hart et al., 1984; for stress analysis of adaptive elastic materials with a view toward
applications in strain induced bone remodelling. Journal of
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Biomechanical Engineering. 106, 342–350.
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pin (Cowin and Van Buskirk, 1978). What is required theories: constitutive modeling and computational aspects. Inter-
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