lnt. .I. Engng Sci., 1973, Vol. 11, pp. 557-565. Petgmon Press.

Printed in Great Britain

ANALYSIS OF BONE AS A COMPOSITE MATERIAL

K. PIEKARSKI
Department of Mechanical Engineering, University of Waterloo, Waterloo, Ontario, Canada

Abstract- Bone is considered to be a composite material consisting of a high elastic modulus mineral ‘fibres’
embedded in a low elastic modulus organic matrix permeated with pores filled with liquids.
Properties and distribution of phases are established or estimated from the experimental data. Theories
of composite materials are applied to bone with various contents of phases, and the discussion summarizes
possible modes of deformation under load. Elastic behaviour is attributed to the joint properties of collagen
and hydroxyapatite. Plastic deformation may occur in the amorphous portions of both mineral and organic
phases. Visco-elastic characteristics are credited to the flow of liquids and viscous deformation of gels and SOIS.

INTRODUCTION
A COMPACT bone is not a homogeneous material, apart from many discontinuities which
will be discussed separately, the ‘solid’ portion consists of substances which have
completely different properties.
The components which have an effect on mechanical properties of bone may be
grouped in the following manner:
1. Crystalline mineral phase - hydroxyapatite,
2. Amorphous mineral phase-composition approximating hydroxyapatite,
3. Crystalline organic phase-collagen
4. Amorphous organic phase -protein molecules in the form of gels and sols,
5. Liquids.
The effect of the above phases on the overall properties of bone depends on the
amount of phases present, their properties and their distribution. At slow rates of
deformation the effect of liquids and sols may be neglected, if it can be assumed that
they can flow freely in and out of a porous portion of bone.
This assumption would justify the replacement of liquids and sols in the list of
structural components with pores.
Further simplification can be made by lumping together crystalline and amorphous
mineral phases for the studies of an elastic modulus of the composite. The elastic
modulus is a structure insensitive property and it can be safely assumed that it has
the same value in the crystalline and in the amorphous mineral phase. The amount of
the amorphous organic phase is very small and for all practical purposes it also may
be lumped together with collagen.
This would reduce the list of components in bone to three:
1. Mineral phase,
2. Organic phase,
3. Pores(filled with liquids).
This simplification allows bone to be visualized as a composite resembling more
familiar engineering materials. The analysis, which follows, will apply to the material
consisting of hard mineral fibres embedded in a soft organic matrix permeated with
pores.
Properties of a composite (bone) depend on the amounts of the components present
as well as properties of individual components.
557

IJ.E.S.Vd. I1 No.6-A
558 K. PIEKARSKI

EXPERIMENTAL MATERIALS

(a) Properties of a mineral phase were not determined experimentally in this study.
(b) To approximate properties of an organic phase, mechanical tests were performed
on various tendons of an adult beef.
(c) To determine mechanical properties of bone the following specimens were
machined:
1. Specimens from haversian bone of a middle third portion of a femur from
an adult steer,
2. Specimens from the same part of a femur from an unborn calf,
3. Specimens from a portion of an inner ear of a whale.
Specimens machined from the first two types of bone were tested not later than a
week after an animal was killed. During that period they were stored in 0.9% saline
solution at 0°C. Special care was taken during the machining operations not to allow
any bone to dry or to be over-heated, so that its properties would resemble as closely
as possible properties of bone in vivo.
An inner ear of a whale was selected because of its very high content of a mineral
phase.
Unfortunately, the bone was not fresh, but in order not to test it dry, it was also
stored for 2 weeks in a saline solution.

STRUCTURAL COMPONENTS OF BONE AND THEIR PROPERTIES

Mineral phase
It has been demonstrated that the mineral phase in bone is that of apatite, more
specifically that of hydroxyapatite CA,,(PO,),(OH),. It has hexagonal crystal structure
with unit cell dimensions a = b = 9.47 A, c = 6.88 A. The most recent investigations
[ 1, 21 suggest that the crystals are rods having diameters of some 20-70 A and extend-
ing in length from some 50 to over 1000 A.
The morphology of hydroxyapatite in a cortical bone is illustrated in Fig. 1. The
organic phase has been digested by prolonged treatment in a 5% solution of collagenese
and further cleaned from the remaining debris in the ultrasonic bath. The fibrous
structure shown is of the mineral phase only indicating that crystallites of the mineral-
ized bone are joined into more massive and continuous structure.
The fact that bone remains in one piece and even displays a very good strength
after an organic phase is removed[3, 41 indicates that the mineral phase must be
continuous.
The mechanical properties of hydroxyapatite are very little known and it will be
necessary to make a series of assumptions and speculations.
Bhimasenacher[S] reported that the elastic modulus of apatite was E = 11150
kg/mm2: Currey[6] estimated it at E = 17600 kg/mm2. Sweeney[4] and Mack[31 have
tested properties of bone with the organic phase removed. Typical values of these
experiments are shown in Table 1.
The values in Table 1 can be converted into values for a solid mineral assuming
that porosity is about 62 per cent and relationships developed for porous ceramics
apply to the porous hydroxyapatite. According to Ryskewitch [7] strength (a) decreases
exponentially with porosity

u = u. exp (- nV) (I)

Fig. 1. (a) Continuous structure of hydroxyapatite with collagen removed of endosteal bone of
a femur of a rabbit x 1250, (b) The same specimen showing mineral structure around lacunae
x 6500.
 Analysis of bone as a composite material 559

Table 1. Strength and elastic modulus of bone with organic phase

removed

Investigator Tension Compression

(Tkg/mm2 E kg/mm* (Tkg/mm2 E kg/mm2

Sweeney 0.690 3.16 780

Mack 0.596 1755 4.80 683

where n is in the range 4-7 and I/ is the volume fraction of porosity.

The elastic modulus, according to Coble and Kingery[8], changes with porosity
following the expression:
E = E,( 1+ 1.9V+0.9V2). (2)
Applying the above relationships, the mechanical properties of hydroxyapatite in
tension can be estimated as follows:
cr = 1l-l 13 kg/mm2, E = 10600 kg/mm2.
However, the absolute value of the modulus of bone apatite still remains a matter for
conjecture and, for the present purpose, it may be assumed that the value due to
Bhimasenacher[S] is suitable as a basis for discussion and that the elastic modulus
of hydroxyapatite is E = 11150 kg/mm*.

Organic phase
This phase consists approximately of 99 per cent collagen. Collagen is a product
of the polymerization of amino acids, the main groups being hydroxylysine and
hydroxyproline. The single polymerized polypeptide molecule has a left-handed helical
shape and this chain in turn twists into a right handed super helix. Three super helixes
form a fundamental unit of collagen structure - a collagen fibril.
The fibrils of collagen also grow into more solid structure and are intimately
connected with the mineral phase. The morphology of collagen, therefore, can also
be illustrated by Fig. 1.
Static mechanical properties of collagen as estimated from the tests on tendons are
as follows:
Ultimate tensile strength 4.5-6.0 kg/mm2
Total elongation 20-30 per cent
Elastic modulus (measured at the steepest portion of the curve) 150 kg/mm2 (max)
It was also found that when a constant strain is applied to a specimen, load reiaxes
asymptotically to some intermediate value. Upon unloading a specimen, strain recovers
in time. The recovery is complete for very small loads, but permanent deformation
occurs if loads are greater than about 1 per cent of the ultimate strength of a tendon.

Pores
The porosity of cortical bone consists of blood vessels (Haversian canals) inter-
connected by canalliculi with lacunae. According to Frost[9] this occupies 13.3 per cent
of volume for a human bone. However, true porosity must be much higher because it
560 K. PIEKARSKI

is possible to evaporate liquids from bone yielding value for porosity equal to 18 pei
cent. In addition, it should be realized that liquids which normally fill pores could not
all be evaporated. The solid portion of the liquids consists of organic and mineral ions
plus large amounts of various protein molecules. Therefore the actual value of porosity
will be well above 18 per cent but this figure has not been estimated and used for this
study, instead, volume of pores was calculated only by evaporation of liquids from bone.

Bone
Mechanical properties of an adult beef bone were fully investigated but for the
purpose of this paper only values of an elastic modulus in tension and porosity are
reported in Table 2.

Table 2. Porosity and elastic modulus of bone specimens

Porosity % E kg/mm*

Standard Standard
Specimen Average deviation Average deviation

Unborn calf 21.3 0.8 593 75.0

Adult beef 18.9 0.45 2045 147.5
Whale 32.4 1.02 3000 65.0

APPLICATION OF THEORIES OF COMPOSITE MATERIALS TO BONE

Most engineering theories have been developed for two phase materials, specifically
for materials having fibres embedded in a soft matrix (fibre reinforced materials).
Bone as described above may have been considered as such a material if it were not
for its high porosity. To study specific mechanical property such as an elastic modulus
it is developed for ceramics (equation 2). Further, information-which is essential for
an analysis of a composite material is the volume fraction of phases in a solid portion
of bone and their spatial arrangement. The volume fraction of a mineral phase was
found by decalcifying bone specimens calculating the weight fractions of phases and
converting into volume fraction by assuming density of mineral phase p = 3.218 g/cm3
and density of organic phase p = 1.14 g/cm3. The data resulting from the above cal-
culations is listed in Table 3. The elastic moduli of three types of bone are now
compensated for porosity and represent a hypothetical value for bone with no porosity.
The arrangement and the orientation of fibres in bone is very complex. The orienta-
tion of fibres in individual osteons ranges from 0 to 45” with relation to the axis of
an osteon[2]. The orientation of osteons with relation to the long axis of bone varies
greatly being however predominantly parallel. The complexity of this structure does

Table 3. Mineral content and elastic modulus of a solid

portion of bone specimens

Volume fraction of A hypothetical value

mineral in a solid of E (kg/mm*) for
Specimen portion of bone bone with no porosity

Unborn calf 0.353 987

Adult beef 0.506 3060
Whale 0.901 6320
 Analysis of bone as a composite material 561

not allow reasonable estimation of the distribution of loads carried by collagen and
apatite fibres. In such cases enginee~ng techniques rely on the use of structural models.

ANALYSIS OF STRUCTURAL MODELS

In order to simplify the mathematical interpretation of the behaviour of the com-
posite, the three elementary models will be considered (Fig. 2). Voigt model of uniform
strain (a) and Reuss model of uniform stress (b) establish respectively the upper and
the lower boundaries for the elastic constants of a composite.
(a) The upper boundary (Voigt)
E,= (E,V,+E,V,+E,I/,+.*..), (4)
(b) the lower boundary (Reuss)

-=1 $l+2+2+. . * .

EC ( 1 2 3 1

where E is the elastic modulus and V is the volume fraction of a phase.

Assuming that the Poisson’s ratio of the components equals zero, the equations
may be used for any number of phases.
Hirsch [ IO] proposed a model (c) which combines (a) and (b) and it can be shown
that it is actually a summation of equations (4) and (5) for a two component system.
I
l
E, = x VIE, -I- V,E;,
)+ (I-x)($2) (6)

where x and 1 -x are the relative proportions of material conforming with the upper
and lower boundaries solutions. According to Hirsch x = 0.5 for concrete.
More accurate predictions of the elastic properties of a composite can be made from
a model proposed by Hashin and Shrikman[ 111

VZ
G,=G,+ 1
6(K,+2GJl/‘r *‘*‘*
Gz-G,+S(3KI+4G~)G,

+
c 1
(a) (b) (cl
Fig. 2. Simplified structural models for the composite material, (a) upper boundary, uniform
strain,(b) lower boundary, uniform stress, (c) Hirsch’s model.
562 K. PIEKARSKI

where K, G and V are bulk modulus, shear modulus and volume fraction of phases.
The upper bound solution is obtained by interchanging K1 and K2 and G, and G,.
The Hashin and Shrikman model and also other models proposed by many investi-
gators who are relating shear and bulk moduli are more difficult to apply to bone
because of the lack of the pertinent data for collagen and hydroxyapatite.
The data from Table 3 were used to plot a graph in Fig. 3. The straight line (a) is
the solution of the upper boundary according to the uniform strain model, equation (4).

0 20 40 60 60 100
PERCENT MINERAL
Fig. 3. Elastic modulus of bone as a function of mineral content, (a) upper boundary (uniform
strain model), (b) lower boundary (uniform stress model), (c) Hirsch’s model for x = 0.925.
Experimental points@.

The lower boundary solution for the uniform stress model is curve (b). The three
experimental points taken from the three types of specimens used, lie between the two
boundaries.
Hirsch’s model applied quite closely to bone x = 0.925. Since the coefficient x is
defined as a relative proportion of the material conforming with the upper boundary
solution, the high value of x for bone indicates that most of the organic mineral phases
are arranged in bone in such a manner that deformation occurs predominately under
uniform strain conditions.
Studies on bone fracture [ 121 indicate that plastic deformation at higher loads occurs
at interlamellar interfaces or in interstitial bone. Fractometry shows pull-out’s of
individual osteons as well as fibrous character of the matrix. This aspect adds another
dimension to the composite structure of bone. Haversian bone on a macro level may
be considered as consisting of osteons (fibres) embedded in an interstitial bone (matrix)
or on a micro level as hydroxyapatite fibres in an organic matrix of solids, gels and SOIS.
In both cases an accurate analysis is rather difficult.

DISCUSSION
The interpretation of a structural model should be made with many reservations.
Since it was only possible to vary the ratio of mineral/organic phases over a limited
 Analysis of bone as a composite material 563

range any conclusions are bound to be speculative. Even more important is the fact that
the microstructure of an inner ear of a whale, which has not been examined micro-
scopically, probably is quite different to the microstructure of a Haversian bone of
a beef femur. However, although the analysis of a structural model of a bone does not
permit the establishment of a fully self-consistent theory of the mode of deformation,
it still provides very significant information. Taking into consideration all assumptions
and inaccuracies it may be concluded that bone is primarily a strain sensitive material.
To discuss in detail the mode of deformation of bone three distinctly different
mechanisms should be considered separately:
(a) fully elastic (Hookean),
(b) damped elastic,
(c) plastic or viscous.
The Hookean behaviour has been questioned by some investigators, but firm
conclusions cannot be made since reported deviations were so close to the possible
experimental errors that it should still remain disputable. On the basis of experimental
evidence in this study it seems reasonable to assume that bone deforms elastically at
low stresses and at high rates of strain.
Both the structural model and microscopic observations suggest that bone does
indeed contain continuous phases which are capable of such elastic behaviour. The
mineral phase (both crystalline and amorphous) would certainly be expected to display
Hookean elasticity. The collagen in its normal (free) state might be expected to show
non-linear elasticity but the experiments suggest that, when incorporated into bone,
such possible behaviour does not occur; though it is uncertain whether this is a true
physical effect (i.e. due to an effective bonding with apatite) or whether its contribution
to load carrying is so small that its behaviour is masked by that of the apatite. Certainly
at the strains normally experienced by bone the strain in the collagen is very low and
it can be considered to display linear, Hookean, elasticity.
A time dependent behaviour is clearly shown by the retardation and recovery
experiments performed on the specimens made from adult beef bone. In view of the
above conclusions this cannot be ascribed to the collagen and it seems likely that,
structurally, the explanation lies in the presence of liquids (including ~01s) in the pores
of bone. The flow of liquids through a continuous network of pores would exert a
damping effect at higher strain rates.
Plastic deformation is not yet fully documented and again it is only possible to
speculate. There are several ways in which unrecoverable plastic deformation may
occur in bone and since they are not mutually exclusive, it is likely that any (or all)
may operate under particular conditions.
A true plastic flow may occur in an amorphous part of both mineral and organic
phases. The amorphous organic phase would certainly flow under quite low stresses
and, if its structure approximates to that of a true gel, it would have a fairly well defined
‘yield point’ at which flow starts. It is conceivable to envisage plastic deformation also
in collagen. Imperfectly or inadequately crosslinked collagen can act independently
of the apatite crystals and deform irreversibly under relatively low stress. This may
occur within the collagen itself or at the interface between collagen and hydroxyapatite.
When load is removed, the mineral phase would remain in strained condition which,
in uivo, can be relieved by the remodelling process. It is a little more difficult to con-
ceive of plastic flow in crystalline hydroxyapatite at the loads involved. It is not
564 K. PIEKARSKI

impossible of course that microfracture of individual crystallites occurs, thus permitting

bulk flow in a material which is not fully coherent[ 131. However, if such a mechanism
does occur in viva, the cracks must presumably be repaired as frequently as they form,
The above analysis applies only to the solid portion of bone. It should be kept
in mind that deformation of this solid portion under stress affects directly flow of
liquids which occupy approximately 25 per cent of bone by volume. Liquids in bone
such as blood and extracellular substance serve as transport media. They supply
the necessary material for remodelling of bone, take away discarded material and carry
nutrients to cells. The effect of stress on the motion of liquids in bone is a subject of
a separate study which is presently under way and will be reported at a later date.

Acknoct&dgement-The author wishes to express his gratitude to Dr. W. D. Biggs for his valuable advice and
constructive criticism of that portion of work which was performed at the University of Cambridge, England.

REFERENCES
[I]M. L. KAY, R. A. YONG and A. S. POSNER, Nature, Lend. 204, 1OSO(1964).
[2] A. ASCENZI, E. BONUCCI and D. S. BIOCCIARELLI,J. Ultrastruc~. Res. 12,287 (1965).
[3] R. W. MACK, Internal Publication, University of California, San Francisco (1964).
[4] A. W. SWEENEY et al., A.S.M.E 65WA/HUF-7, New York (1965).
[5] J. BHIMASENACHER, Proc. Zndiun Acad. Sci. 22A, 209 (1945).
[6] J. D. CURREY, Biorheology 2, 1(1964).
[i’] E. RYSKEWlTCH,J. Am. Ceram. Sot. 36(2), 65-68 (1953).
[S] R. L.COBLEand W. D. KiNGERY.~.Am.Cerarn.S#~.39,377(19S6).
[9] H. M. FROST, Henry Furd. Hosp. med. Bull. lo,35 f 1962).
[IO] T. J. HIRSCH,Proc.Am. Concr. Inst. 59,427 (1962).
11I] T. HASHIN and S. SHTRIKMAN, J. Me&. Phys. Solids 11,127 (1963).
[12] K. PIEKARSKI, J. Appl. Phys. 41,215 (1970).
[ 131 H. L. FROST, Henry Ford Hosp. med. Bull. 8.25 ( 1960).
[I41 U.Y.COUNTO,Mog.Concr.Res.16, 129(1964).
[ 151F. G. EVANS, Stress and Strain in Bones. Thomas (1956).
[ 161 R. H. HALL,J. Sue. Leather Trades Chem. 36, 137 (I 9.52).
[ 171 H. K. KRECHNEL, Fibre Reinjkcement, Land. Skand. Forlag (1964).
[ 1S] J. K. MACKENZIE, Proc. phys. Sot. 63B. 2 (19SO).

Resnmi-On considere que 1’0s est un mat&au composite consistant en des “fibres” min&ales au module
elastique Cleve incluses dans un milieu organique, de faible module Clastique, poreux et dont les pores sont
remplis de liquides.
Les proprietes et la distribution des phases sont dtablies ou estimees a partir des don&es experimentales.
Les theories de materiaux composites sont appliquees a 1’0s avec differents contenus des phases et la dis-
cussion resume les modes possibles de deformation sous une charge. Le comportement elastique est attribue
aux proprietes reunies du collagene et de l’hydrozyapatite. Une deformation plastique peut avoir lieu dans
les parties amorphes des phases minerales et organiques. Les caracteristiques visco-elastiques sont attribuees
a l’ecoulement de liquides et a la deformation visqueuse de gels et de sols.

Zu~~en~~u~ - Bein wird als zusammengesetzter Stoff betrachtet, der aus Mineralfasem hohen efas-
tischen Moduls besteht, die in eine organische Matrix niedrigen elastischen Moduls eingebettet sind, die van
fliissigkeitsgefiillten Poren durchdnmgen ist.
Eigenschaften und Verteilung der Phasen werden von experimentellen Daten erhalten oder geschatzt.
Theorien zusammengesetzter Stoffe werden auf Bein mit verschiedenen Phaseninhalten angewandt, und die
Diskussion gibt einen Uberblick iiber miigliche Deformationsarten unter Belastung. Elastisches Verhalten
wird auf die vereinigten Eigenschaften von Kollagen und Hydroxyapatit zuriickgeftihrt. Plastische Defotma-
tion kann sich in den amorphen Teilen sowohl mineralischer als such organischer Phasen erreignen. Visko-
elastische Kennzeichen werden auf die Striimung von Fhissigkeiten und viskose Deformation von Gelen
und Solen zu~ckge~h~.

Sonsmario-L’osso t ritenuto un rnateriale compost0 consistente in “tibre” minerali con module di alta
elasticim allettate in una mat&e organica di bassa elastic&a permeata di pori riempiti di liquidi. Si stabiliscono
o si valutano in base a dati sperimentali le propried e la distribuzione delle fasi. Si applicano teorie di materiali
 Analysis of bone as a composite material 565

composti all’osso con vari tenori di fasi e nella discussione si fa un sommario dei modi possibilidi defor-
mazione sotto carico. Si attribuisce comportamento elastic0 alle proprieta miste dell’osseina e dell’idros-
siepatite. Si possono avere deformazioni plastiche nelle porzioni amorfe delle fasi sia minerale sia organica.
Alflusso deiliquidieladeformazione viscosadeigele dei solsiimputano caratteristichetermoelastiche.

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