J. Biomechanics, 1975, Vol. , pp.393405. Pergamon Press.

Printed in Great Britain

THE ELASTIC AND ULTIMATE PROPERTIES OF

COMPACT BONE TISSUE”?

DONALD T. REILLY and ALBERT H. BURSTEIN

Biomechanics Laboratory, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, Ohio
44106, U.S.A.

Abstract-The use of a transversely isotropic model is tested for the elastic behavior of bovine and
human bone and the five independent constants of this model are determined. The accuracy of the
model is tested for eight cases by comparing the off-axis modulus predicted by a rotation of stiffness
matrix with an experimentally determined off-axis modulus.
Ultimate properties are presented for bovine and human bone for tension, compression, and
torsional loads. A Hankinson type failure criterion is proposed for off-axis ultimate stress and this
predicted value compared with experimental values for nine cases.

INTRODUCTION gated by three point bending of machined cortical

The elastic and ultimate characteristics of bone
are a description of the response of the tissue, in a
mechanical sense, to stress incurred as it performs
its biologic structural function. Those loading
cycles that do not cause permanent irreversible
changes occur within the region of elastic tissue
behavior. The response of the tissue in this region
to external loads, that is, the relation between
deformations and applied forces, is characterized
by the “elastic constants”. In order to describe the
mechanical response of bone in the elastic range,
Lang (1970) postulated a five elastic constant or
transversely isotropic model for the elastic nature
of bone and determined the constants using an
ultrasonic technique. A transversely isotropic
material exhibits one set of elastic properties in one
direction and a second set of elastic properties in
the two directions (or plane) perpendicular to that
direction. Past work on the anisotropic mechanical
properties of bone is difficult to compare consider-
ing the varying methods of testing and is summar-
ized in the review by Reilly and Burstein (1974a).
Since very little plastic deformation was shown in
all work previous to Burstein and others (1972), one
can directly criticize the ultimate values obtained.
Indirectly, one could speculate that since the bone
specimen was not wet enough to undergo plastic
deformation, its elastic properties might also have
been altered.
One recent paper by Pope and Outwater (1974)
bears special mention since it concerns itself with
the topic of this paper yet contains serious
misconceptions in its approach to the testing of
both elastic and ultimate properties of bone.
Mechanical properties of bovine bone were investi-
*Received 2 August 1974.
t This investigation was supported by an NSF Grant
No. GK-37023X; NIH Grants, Nos. Hd-00669-11; and AM
16058-02; and NFWO Grant No. S. 2/S-A.O.G./JO.E6Z.
specimens. Analysis of the load-deformation of the
specimens was done using linearly elastic beam
theory. This brings up two problems. First, in the
choice of specimen dimensions the authors have
introduced the problems of biaxiality. The only hint
of specimen dimensions was given when they
claimed that the biaxial stress problem was reduced
by maintaining the “thickness/width ratio (set)” at
<2.7 following the recommendations of Weiss
(1960).” Weiss made no such recommendations but
merely gave a graph showing how biaxiality varied
with width/thickness change. In fact, at a
width/thickness of 2.7, he showed that the problem
of biaxiality is reduced by only 30%. Biaxiality can
only be minimized when the thickness and width
are equal. Secondly, linearly elastic behavior has
been shown to be completely inadequate for wet
bone by Burstein and others (1972) and gives rise to
errors of from 50 to 100% for ultimate strength.
Pope and Outwater stated that the problems due to
plastic deformation were “substantially reduced by
running at a higher strain rate than Burstein and
others must have used”. No data are presently
available on the strain rate sensitivity of plastic
deformation of fresh bone. The only available data
are those of McElhaney and Byars (1956) who
reported on the strain rate sensitivity of embalmed
femoral bone. These specimens were small cubes
tested in compression. It is of particular interest to
note that a comparison of the curves of specimens
tested at strain rates of 1lsec and 0.1 lsec showed no
different load deformation behavior. The reported
strain rates of Pope and Outwater (1974) were
2/set while those of Burstein et ul. (1972) used
strain rates that were approximately O.l/sec.
Finally, Pope and Outwater presented no load
deformation data to support their interesting
contention of a reduction in plastic deformation
with an increase in strain rate.
In their anisotropic strength model. Pope and
394 D. T. REILLY etal.

Outwater took some unfounded steps. They at-

tempted to develop a formulation for the fracture
stress as a function of the angle rotated from the
long axis of the bone. They substituted their
experimental values for strength ,derived from
bending tests into this formula which they clearly
stated assumes uniaxial tension strengths. This
formulation was further confused by their substitu-
tion of an ultimate shear strength value for wet
human femur where a value for their tested bone
type (bovine tibia) was called for. Hence, while
their topic was an important one, their exposition
X-longitudinal
was unclear and unsound. Y-Transverse
This study has five specific objectives: Z-Radial

Fig. 1. Cartesian coordinate system chosen for cortical

Elastic properties
bone specimens.
1. To verify the existence of an isotropic plane,
perpendicular to the long axis of the bone for
bovine Haversian bone and therefore, the suitabil- Haversian or laminar type. Bones with a cortex too thin to
ity of a transversely isotropic model for this produce the 5 mm outside dimensions of the above
specimens were cut into long rectangular parallelepipeds
histological bone type.
(square cross section of approx. 3 mm) and used for
2. To determine the five elastic constants for a torsion tests for the shear modulus.
transversely isotropic model for bovine and human The nonlinear response of the material in the torsion
bone. tests necessitated round cross section specimens for the
3. To test the accuracy of the transversely determination on the ultimate torsion strength (see section
below on torsion testing). The 5 mm square cross section
isotropic model by predicting the elastic modulus parallelepipeds were used for fabrication of these
expected in off-axis tension and compression tests. specimens. They were placed in a small lathe and a
reduced section was turned under a constant water flow
Ultimate properties (Fig. 2).
4. To determine the ultimate properties of Haversian bone with its osteons oriented in a preferred
direction has an axis of symmetry and therefore,
human and bovine bone tissue and the variation of histologically, an isotropic plan perpendicular to this axis
these properties in different directions. of symmetry. We attempted to fit the transversely
5. To formulate a failure criterion for uniaxial isotropic material model (five independent constants) to
tension or compression loads. the inherent histological symmetry. Figure 3 shows an
idealized block of Haversian bone with the chosen
Cartesian coordinates. The longitudinal direction is along
the osteonal axis and according to the transversely
MATERIALS isotropic model, the elastic modulus (E) and Poisson’s
Specimen preparation ratio (u) in the plane perpendicular to the longitudinal
Specimens were machined from the cortex of the direction should be the same regardless of specimen
middle third of fresh frozen long human and bovine orientation. Therefore, to test the transversely isotropic
bones. Since mechanical properties were determined as a model, specimens were cut in the isotropic plane (y-z) for
function of direction, a reference system had to be chosen bovine Haversian bone. (The required size of the
for the orientation of the specimens in the cortex. The
Cartesian coordinate system chosen (Fig. 1) takes the
x-axis parallel to the long axis of the bone and a specimen
machined with its long axis in this direction was termed a
longitudinal specimen. The y-axis was the circumferential
direction while the z-axis was the endosteal-periosteal
direction. Specimens with their long axis in the y direction
are called transverse specimens and specimens with their
long axis in the z direction are called radial specimens.
Off-axis bovine specimens were also prepared with their
long axis in the x-y plane and y-z plane at angles of 30”
and 60” to the x-axis and y-axis respectively. Bone
specimens from both human and bovine bones were
prepared by first thawing frozen bones following the
procedure outlined by Reilly and others (1974b). At the
rectangular parallelepiped stage of fabrication, the his-
tological types of bovine bone was checked. Both ends of
the 15 mm block were ground flat and stained with
brilliant green stain to highlight structure. If a mixed type
of histology was noted (at 30x) a final specimen was not
milled. As we have noted previously, the possibility of a
strain concentration at interfaces between different
histological bone types may prejudice the results.
Therefore, bovine bone values are for completely Fig. 2. Dimensions for the circular torsion specimen.
 The elastic and ultimate properties of compact bone tissue
x gage length of the extensometer. The extensometers were
t gages in a four element bridge. They were designed to be
,0steon
Fig: 3. Orientation of x-y-z axes with respect to the
osteon systems.
specimens precluded this test in human cortical bone).
The longitudinal specimens gave two more of the
independent constants E’ and Y’. Tension and compres-
sion tests at a strain rate of 0.02-0.05 see-’ were
performed on longitudinal, transverse, radial and inter-
mediate angle (30” and 60”) specimens taken from the
plane of isotropy and the x-y plane.
METHODS
Testing machines
Uniaxial tension or compression testing was done on a
testing machine incorporating a loading pendulum on a
shaft to which a displacement cam was attached described
in Reilly and others (1974b). Torsion tests were run on a
testing apparatus described by Burstein and Frankel
(1971).
When possible, a “case” consisted of specimens from a
single bone. If enough specimens from a single bone were
not available to warrant a statistically meaningful group,
specimens from several bones were combined (noted in
Tables). For instance, the approximately twenty speci-
mens needed for an off-axis type of test might come from
three bones with cortical material randomly assigned to
the four directional (0”. 30”, 60”, 90”) groups.
Extensometers were used for the determination of both
longitudinal and transverse (Poisson’s) strain on longitudi-
nal, transverse, and radial specimens. Only longitudinal
strain was measured for off-axis specimens. Strain was
calculated by dividing the change in dimension by the
Fig. 5. The Poisson’s extensometer shown in detail. The
dowel pins allow the extensometer to hang from the bone
specimen while recording change in width in only one
direction.
395
instrumented with 2000 Cl semiconductor type strain
clipped to the specimen gage length quickly and their
attachment did not entail any procedure which would
change the bone specimen surface (e.g. gluing or drying),
and thus could be used on wet bone. The extensometer
used for longitudinal strain measurement (strain in the
direction of the tensile or compression forces) was
described by Reilly and others (1974b).
The extensometer used for Poisson’s strain (v’ for
longitudinal loading and v for transverse loading) ‘is
shown in Fig. 4 on the left hand side. Here again the spring
steel clip portion, instrumented with strain gages, afforded
a light preload against the specimen. Two steel dowel pins
were used so that Poisson’s strain in the perpendicular
direction would not be constrained or load the extensome-
ter. Any Poisson’s strain in the direction perpendicular to
that of interest would. only cause rotation and not
deflection of the extensometer due to jaw design shown in
Fig. 5.
DATA RECORDING AND REDUCTION
Recording of data from the load cell and extensometers
for the tension and compression tests were done on a
storage oscilloscope. A photograph of the trace was then
taken.
A stylized and an actual load deformation curve for a
tension test of a longitudinal specimen are shown in Fig. 6.
Straight lines were fitted by eye to the two portions of the
curve and the following points used for reduction of the
data. The point of intersection of the two fitted straight
lines were chosen as the yield point. This method was
convenient and gave repeatable results for the yield point
which represented approximately the same value as a
0.2% offset strain method. The stress at this point was
found by dividing the load (on the vertical axis) by the
original cross sectional area of the specimen and is
hereafter called the yield stress (u>).
The slope of the straight line from the origin to the yield
point was used for determination of the elastic modulus
(E’ in longitudinal direction, E in transverse direction)
after appropriate conversion of load and area to stress and
deformation to strain.
The slope of the second straight line fitted to the load
curve again expressed as the ratio of stress to strain was
used for the determination of what was defined as the
“strain hardening modulus” (S), a term borrowed from
the engineering description of metallic behavior.
The ultimate stress (u..) was found from the highest
load (P..) carried by the specimen before fracture.
divided by the initial cross sectional area. Ultimate strain
(E.,,) was calculated from the deformation undergone to
the fracture point (IL.,,) divided by the initial length of the
specimen gage section.
Similarly a stylized and an actual load deformation
curve is shown for a compression test of a longitudinal
specimen in Fig. 7. The initial portion of the curve was
fitted by eye with a straight line whose slope represented
the elastic modulus (E’ or E) with appropriate transfor-
mation to stress and strain.
The ultimate compression stress (u,,J was found from
the highest load supported by the specimen before
fracture divided by the initial cross sectional area. Many
of the human specimens tested had the type of curve
shown in Fig. 7 for compression load-deformation and the
problem of ultimate strain determination arose since the
continued horizontal deflection of the trace represented
impaction of the fracture pieces after the highest load
point. The ultimate compressive strain to fracture was
therefore defined as that strain calculated from the
displacement undergone by the specimen when it
supported the highest load.
The shear modulus was determined using a torsional
3% D. T. REILLY et al.
test. A straight line fitted to the initial slope of the torque
displacement curve represents the product of the shear
modulus (G’) and the torsional constant (.I).
Thus:
$= G’J,
where T = torque and 0 = angle of twist per unit length.
For the circular cross sectional specimens, the value for _I
is simply the polar moment of inertia (&rr4, where r was
the radius). The torsional constant for the nominally
square cross section however was approximated by:
J = 16a3b $-StanhE ,
>
where a = half of smaller dimension of cross section and
b = half of larger dimension of cross section, after Wang
(1953).
Determination of the ultimate shear strength in the
torsion test when the material behaves in a linearly elastic
fashion is not difficult. Linear elastic response was found
to be the case for the torsion test when laminar bovine
bone was used. Then the shear stress (which for the
rectangular cross section would be highest at the midpoint
of the longest side) was found using the series given by
Wang (1953):
T~x=~[1-~(“~~(2n+I)‘lcoshkb)] n Also an analysis of variance for the data for the
where r,,. = maximum shear stress, k,, = (2n + 1)/2a,
T = torque at failure and .I, a and b, are defined above.
The validity of the torsion test to determine shear
strength and the points of maximum shear stress have
been discussed by Burstein and others (1973).
Torsional tests performed on human and bovine
Haversian bone specimens showed the material had a
nonlinear torque versus angular deformation curve.
Determination of the shear modulus as described above,
was taken from the initial slope of the curve. The ultimate
shear stress, however, was found using the elegant
solution described by Nadai (1950). This solution holds
only for the circular cross section and entails a graphical
interpretation of the load-deformation curve but is an
exact solution given as:
where a = radius of specimen, 0 = angle of twist/unit
length and M = torque at fracture. Then from a torque
deflection curve (Fig. 8) Nadai showed:
&$(Me’)=@+3M,
where D is taken from load deformation curve
as in Fig. 8.
In those tension or compression tests in which
Poisson’s ratiojvas found, the load deflection curves for
both longitudinal and transverse strain were displayed on
the same oscilloscope screen through a dual channel input
(Fig. 9). The trace on the left hand side is the familiar load
(vertical axis) vs deformation in the direction of the load
(horizontal axis) while the trace on the right hand side
represents, simultaneously, load (vertical axis) vs defor-
mation perpendicular to the direction of the load
(horizontal axis). Positive is to the right and hence the
deflection here requests a reduction in cross sectional area
under a tensile load. A straight line was fitted by eye to
this curve and the ratio of the reduction in width to
Angle of twist/unit length
Fig. 8. Torsional load-deformation curve showing graphi-
cal solution. After Nadai (1950), see text.
elongation at the same load below the yield point gave
Poisson’s ratio.
RESULTS
Elastic properties
The results of the experiment for the initial
objective of verifying the isotropic plane in bovine
Haversian femora (y-z plane) are shown in Table
1. A comparison of the constants in the transverse
and radial direction with a t-test show no significant
difference (at the P < O-05 level) for both E and u.
four directions showed no significant added var-
iance (at the P < 0.05 level) for the two elastic
constants. Thus, the values of the elastic constants
for all directions in the y-z plane are not shown to
be different and the y-z plane is a plane of isotropy
or has constant elastic properties regardless of
direction of load in that plane.
The results of the experiments for the second
objective, the determination of the five constants,
E, Y, E’, v’ and G’ are shown in Tables 2 (human)
and 3 (bovine). The value given for the shear
modulus (G’) in Case X represents an overall mean
for all torsional specimens of human bone.
If a material behaves in a transversely isotropic
manner, the elastic modulus for specimens cut in
the x-y plane at an angle C#Jto the x-axis (Fig. 10)
can be found for uniaxial load by the equation:
Therefore by determining the five elastic constants,
we could calculate the off-axis moduli. Figures
II-18 represent the results of these experiments.
The solid line represents the values for E(4)
calculated using the above expression and the mean
values for the elastic constants. The dotted line
represents the E(4) calculated using constants one
standard deviation from the mean. Experimental
points are shown on the graphs with one standard
deviation in each direction. The values and number
of specimens for each experimental point are given
in the Appendix. Both tensile and compressive
determinations are shown.
 The elastic and ultimate properties of compact bone tissue 397

Table 1. Bovine. Haversian femur

ELASTIC PROPERTIES
Tension in Isotropic (y-z) Plane
E
Direction n ix10gN/m2) "

Transverse 4 12.0(4.62) .45(.250)

3o" 7 LL.3(3.19) .47(.106)

60' 4 10.6(1.69) .34(.071)

Radial 6 10.0(0.50) .44(.040)

ENTRIES IN TABLES ARE GIVEN AS: NEAN(St.Dev.)

n - number of specimens

E = elastic modulus for transverse or radial specimens (in y-z plane)

E' = elastic modulus for longitudinal specimens (in x direction)

G' = shear modulus

" = Poisson's ratio for transverse or radial specimens

Y' = Poisson's ratio for longitudinal specimens

S = strain hardening modulus

'Jult = ultimate stress

= yield stress
=Y
= strain at fracture
EUlt

Table 2. Human femur

ELASTIC PROPERTIES

TENSION E E' C'

Case (x10gN/m2) n u n (x10gN/m2) n Y' n (xLOgN/m2) n
I* 10.1(2.35) 6 .62(.257) 5 17.9(3.92) 15 .40(.157) 13
IIf 14.1(3.31) 7 .45(.173) 7 18.3(4.57) 12 .51(.183) 12
III (right)+ 13.2(2.87) 7 .51(.264) 7 15.6(2.74) 5 .35(.203) 5 3.71(.467) 6
IV (Left)+ 13.4(3.34) 5 .59(.x22) 5 17.9(3.22) 6 .29(.025) 6 3.10(.379) 4
XU 3.28(.383) 166

COMPRESSION
v* 11.7(101) 5 .63(.197) 5 lS.Z(O.85) 4 .38(.154) 4

* Composite of bones aged 41 female, 49, 61, 71 males

** 21 year male
+ 23 year male
+t Specimens from 15 male, 5 female - ages 21 - 86

Table 3. Bovine femur

ELASTIC PROPERTIES

R2 E' G'
MVRRSIAN (xlO'N/m ) n Y n (x10gN/m2) n Y' n (xlO'N/m*) n
Tension

case VI 10.40.64) 5 .51(.236) 5 23.1(3.18) 3 .29(.079) 3

Compression 3.57(.250) 22
case VII lO.l(l.78) 8 .51(.115) 8 22.3(4.61) 5 .40(.209) 5

LAMINAR
Tension
case VIII 11.0(.173) 25 .63(.226) 6 26.5(5.37) 6 .41(.2m) 10 5.09(.389) 6
 Fig. 4. Compression test set up. Both longitudinal and Poisson’s strain extensometers are shown in
place.

(Facingp. 396)
 Tension Compression

Fig. 6. Actual and idealized tension load-deformation Fig. 7. Actual and idealized compression load-
curves. The lower drawing shows how data points were deformation curves.
interpreted from photographic data recordings.
 Fig. 9. Load-deformation curves for tension tests with Poisson’s strain recorded. See text.

Fig. 19. Load-defiection curve from a compression test on a transverse specimen from a human fe
398 D. T. REILLY et al.

Fig. 10. Off-axis specimen orientation to coordinate

systems.
0 30 60 90

Angle ‘P, deg

Fig. 13. Case III. Off-axis modulus determined from a

tension test on human femoral specimens.

i I I I I , ,

Fig. 11. Case I. Off-axis modulus determined from a 0 30 60 90

tension test on human femoral specimens. Angle ‘P, deg

Fig. 14. Case IV. Off-axis modulus determined from a

tension test on human femoral specimens.

0 30 60 90

Angle 9, deg Angle ‘P> deg

Fig. 12. Case II. Off-axis modulus determined from a Fig 15. Case V. Off-axis modulus determined from a
tension test on human femoral specimens. compression test on human femoral specimens.

Ultimate properties
Table 4 shows the ultimate properties for tensile
tests in the longitudinal and transverse directions
for specimens from ihe same bone. Included also in
these table are the values for the yield stress (cry)
and strain hardening modulus (S) which relates
stress and strain after the yield stress is reached
The average ratio for the ultimate tensile stress in
the longitudinal direction to that in the transverse
direction is 2.6 for the four individuals studied. The
ultimate strain undergone by a specimen was on the
average of four times higher in the longitudinal
 The elastic and ultimate properties of compact bone tissue 399

Table 4. Human femur, tension

ULTMATE PROPERTIES

specimen Oult
BONE orientation n (x106N/m2) EUlt

A+ Longitudinal .038(.0054) 0.637CO.1526) 113.(8.7)

Transverse : .008(.0013)
III (right)+
Longitudinal 5 .02n(.0071) 0.842(0.4133) 116(11.7)
Transverse 7 .uo7(.0015)

IV (Left)+t Longitudinal 137 11.6) .030(.0059) 0.862CO.1774) 117C7.3)

Transverse ; 62 8.9) .007(.0016)

31" Longitudinal 3 .022(.0044) 1.069(0.0403) lOB(4.5)

Tr.ClnSVerSe 3 .006(.0013)

Mean Value Longitudinal 21 135(15.6) .031(.0072) 0.812(.1470) 114C3.1)

Transverse 20 53C10.7) .007(.0014)

+ 31 year male

+t 23 year male
* 63 year male

4 , . . , 1

4 1 I I . . * 0 30 M) 90
0 30 60 90
Angle(p, deg
Angle9, de9

Fig. 16. Case VI. Off-axis modulus determined from a Fig. 18. Case VIII. Off-axis modulus determined from a
tension test on bovine Haversian specimens. tension test on bovine laminar specimens.

30
1 would result in very low energy absorption
Angle ‘P, deg
Fig. 17. Case VII. Off-axis modulus determined from a
compression test on bovine Haversian specimens.
direction than in the transverse. This would make
the average energy absorbed by the bone tissue in
the longitudinal direction greater than that of the
transverse by one order of magnitude. It is quite
obvious how this type of loading configuration
considering the low stress levels and absence of the
long plastic phase.
The compression tests of human specimens in
the longitudinal and transverse directions did not
produce such great differences. The ultimate stress
in the longitudinal direction (Table 5) was approxi-
mately one and one-half times as great as the
ultimate stress needed for fracture in the transverse
direction. The strains to failure in the transverse
compression tests, however, were larger than those
of the longitudinal tests. With impaction of
fragments and therefore an inability in determining
a precise failure strain (as could be done in the
tension tests), the comparison of ultimate strain and
energy for the two compression tests is more
difficult than in the tension test. However, whatever
criterion is used for the ultimate strain, the energy
absorbed in the two compression tests would not
show the order of magnitude difference of the
tension tests. The transverse compression tests for
some of the Haversian type bone specimens
(human A and bovine 3) gave an interesting
400 D. T. REILLY et al.

Table 5. Human femur, compression

LILTIMATBPROPERTIES

Specimen Oult
BONE Orientation n (x106N/m2) 'ult
A* Longitudinal 6 203C27.6) .019(.0034)
Transverse 3 151C10.7) .087(.0248)
22** Longitudinal 3 198C12.7) .018(.0038)
Transverse 5 lH(13.6) .028(.0029)
1131+ Longitudinal 7 206(10.0) .019(.0029)
1132i+ Longitudinal 4 211C14.4) .018(.0007)

Mean Value Longitudinal 205C17.3)

Transverse 131C20.7)

* 31 Year male

** 52 Year male

+ 21 year male

++ 22 year male

Table 6. Bovine, tension

ULTIMATE PROPERTIES

OUlC s OY
Specime
TYPE/BONE orientation n h106N/m2) 'ult (x10gN/m2) (x106N/m2)
Haversian Bone

Femur 3 Longitudinal .016(.0048) 0.340(.2725) 14OC6.8)

Tra"SVerSe : %I ;:1"; .009(.0011)
Tibia 1 Longitudinal 7 1:;;18":;j .022(.0064) 0.665CO.2179) 141C19.7)
Transverse 5 .009(.0?37)

Femur 9 H Tra"SVerSe .007(.0042)

Radial .007(.0018)

Lamlnar Bone
Femur 4 Longitudinal .033(.0049) 0.767CO.2571) 156C7.9)
Transverse .007(.0012)

Femur 9 L Transverse .008(.0016)

Radial : .002(.0006)

load-deformation curve. Figure 19 is typical of the tension tests of the radial specimens of the laminar
curves obtained from these transverse compression type bone all fractured through the region of
tests. They were similar in form to the curves vascular network, which for these specimens is
obtained from longitudinal tension tests. Since perpendicular to the load direction and produces a
shear cracks and microbuckling were seen in the reduced load carrying area. The ultimate strains for
failed specimens, the mechanism producing the the laminar type radial specimens hence show a
plastic deformation in transverse compression is four fold decrease from the transverse ultimate
therefore different than the tension yield strain. Energy to fracture of the Haversian type
mechanism. specimens is three times higher in the longitudinal
The bovine Haversian specimens used for direction than the transverse direction and about
tension tests (Table 6) showed an approximate 50% higher in the transverse direction than in the
strength ratio for the principal directions of radial direction due to the lower radial ultimate
longitudinal, transverse, and radial of 3 : 1: 0.7. This stress. The laminar bovine bone showed about a
table also shows that for the laminar bone 2:3 ratio of longitudinal to transverse energy
specimens, the ratios of tensile strength for the absorbed to fracture and the transverse energy to
principal directions was about 3 : 1: O-4. The differ- fracture was an order of magnitude greater than
ence in the ratios for the two different histological that in the radial direction due to the vascular
types of bone tissue is due to that very histologic network strain concentration.
difference. The Haversian type showed no differ- Compression of bovine Haversian specimens
ence for the ultimate strain in the transverse and showed an approximate ratio of strengths in the
radial direction since in this plane whether the principal directions of 1.6 : 1: 1 (Table 7).
tensile load is transverse or radial, it is pulling The shear strength of bone tissue as determined
perpendicular to the axis of the osteons. The from the torsional tests are listed in Table 8 for both
 The elastic and ultimate properties of compact bone tissue 401

Table 7. Bovine Haversian femur compression

ULTIMATE PROPERTIES

Oult
Specimen
BONE Orientation n (x106N/m2) Cult

Femur 3 Longitudinal 272( 3.3) .016(.0015)

Transverse a 146(31.8) .032(.0010)

Femur 9 Tral-tSVZXSe 4 196(11.4) .053(.0197)

Radial 5 190(18.0) .072(.0137)

Table 8. Human and bovine shear strength

ULTIMATE PROPERTIES

‘ma Longitudinal "ult

TYPE Bone n (x106N/m2) Tmax

Human Iv* 4 ::I 2:$ 1.9

(femur) 41+ 8 2.2
Bovine
Haversian Cl 3 67( 5.5) 1.7
(femur) C2 4 72(12.0) 1.8
BOVilW
Plexiform Dl 66( 7.8) 2.7
(femur) DZ 6" 62( 6.0) 2.9

* 23 year male

+ 56 year male

human and bovine bone. In the table, the shear
strength is compared to the longitudinal ultimate
tensile strength found for specimens from the same
bone. For human and Haversian bovine bone, the
shear strength was found to be approximately
one-half the ultimate tensile strength, but in the
laminar type bovine bone, it was one-third as great.
This finding can also, we feel, be attributed to the
plane in which the laminar type bone has its
vascular network. A fracture of this type was
described by Burstein and others (1973).
An attempt was made to describe the ultimate
strength of bone specimens under uniaxial loading
at orientations between the principal directions
with an empirical strength criterion. A simple and
convenient type of criterion was introduced by
Hankinson (1921) to describe the ultimate compres-
sive strength of wood. His criterion relates an
off-axis strength to the strengths determined in the
two principal directions as follows:
found for the off-axis specimens used for the
off-axis modulus experiments and are shown in
Figs. 20-27. The solid line represents the predicted
off-axis ultimate stress using the mean values and
n = 2 in the Hankinson formula. Again the dotted
lines are calculated using the mean values with one
standard deviation added or subtracted. Actual
experimental values are included in the Appendix.
Figure 28 is the ultimate stress found for the
specimens used in the isotropic plane elastic
constant experiment, and shows that the Hankin-
son criterion holds for y-z plane also. This case
was run since the transverse ultimate stress was
found to differ significantly (P <: O-05) from the
radial ultimate stress.

S(9O)S(O)
S(4) = [S(90) COS”f#J+ S(0) sin” $1’

where S(C#J)= the off-axis ultimate stress at some

angle of rotation, S(0) = longitudinal ultimate stress
(tensile or compressive), S(90) = transverse ulti-
mate stress (tensile or compressive), I#I= angle of
rotation from principal direction and n = any
number.
If the principal ultimate tensile stresses are used,
this criterion is for the off-axis ultimate tensile
stress and principal ultimate compressive stress
values allow it to be used for off-axis ultimate Fig. 20. Case I. Off-axis strength in tension for human
compressive stress. The ultimate stresses were femoral specimens.
402 D. T. REILLY et al.

36 66 9b 30 60 90

Angle, deg Angle, deg

Fig. 21. Case II. Off-axis strength in tension for human Fig. 24. Case V. Off-axis strength in compression for

\
femoral specimens. human femoral specimens.

15c
\ casem
casem
\
“E

1
2
“0 -1
; IOC ’ \ \ ‘11
\ \
\ \
\
‘1 \,
‘. -___
‘\
---

0’ 3; &J 9b
0 30 60 90

Angle, deg 4m$e, deg

Fig. 22. Case III. Off-axis strength in tension for human Fig. 25. Case VI. Off-axis strength in tension for bovine
femoral specimens. Haversian femoral specimens.

0 - 60 90
Angle, deg
Angle, deg

Fig. 23. Case IV. Off-axis strength in tension for human Fig. 26. Case VII. Off-axis strength in compression for
femoral specimens. bovine Haversian femoral specimens.

CONCLUSIONS or three dimensional investigations. The results of

Many studies dealing with the mechanical be- this study with regard to Haversian bovine bone
havior of bone have assumed linear elastic proper- support the transversely isotropic model of Lang
ties. We no longer feel such a model is valid for two (1970) who found value for the five elastic
 The elastic and ultimate properties of compact bone tissue 403

G’ = 3.6 x lO’N/m* 22
v’ = 0.36 8
v= 0.51 13.

For human femoral compact bone, our overall

mean values were:

E’ = 17.0 x lO’N/m* $0)

E= 11-5x lO’N/m* (31)
G’ = 3.28 x lo9 N/m2 (166)
u’ = 0.46 (147)
v = 0.58 (26).
0 -0

--.
The values for E and E’ are associated with a

--\
Angle, deg
standard deviation of approx. 15-20% of the
Fig. 27. Case VIII. Off-axis strength in tension for bovine modulus if determined in tension and 7-10% if
laminar femoral specimens. determined in compression. Standard deviations
for the Poisson’s ratios were generally in the range
60 of 30% of the ratio. These large ranges are most

I-%
CaseLX likely due to the inhomogeneous nature of the bone
-. material (in porosity, mineralization, and osteonal
‘.
50
? --. . .
direction), and specimen size (presumably a larger
2 -. -L_
--
cross-sectional area would produce a better averag-
h 40
.\
‘.
ing of the local inhomogeneities). The high values
. .
.-._
-_- for the Poisson’s ratio, with many individual
specimens having a ratio greater than 0.5, attests to
30-
the fact that the “material” is really a structure with
a high degree of kinematic deformation. Standard
20- deviations for the shear modulus was approx. 10%
of the values observed.
IO- The validity of the transversely isotropic model
was tested by the attempt to predict the moduli
found in uniaxial tests at angles of 30” and 60” to the
r 1 ,
0 30 60 90 long axis of the bone using the five constants and
Angle, deg matrix rotation. While some predicted values
correspond very well with the experimental off-axis
Fig. 28. Case IX. Off-axis strength in tension for bovine stiffnesses, others (notably Cases III and IV) do
Haversian femoral specimens.
not. This is particularly disconcerting considering
the fact that Case III represents bone specimens
constants as follows:
taken all from one bone and Case IV is the
contralateral side. The discrepancy may very well
E’ = 22.0 x IO’ N/m’
be due to the method of obtaining the specimens
E= 11.3 x lO’N/m* from a single bone. When several bones were used
as the source of specimens for the off-axis tests, an
G’ = 5.4 x 10’ N/m2
attempt was made to obtain at least one of each
v’ = O-48 orientation specimen from each bone used. When a
single bone was used to obtain all orientations of
v = 0.40.
specimens, sufficient numbers could be obtained
only if a specimen of one orientation was taken
His specimens were from the phalanx but he did
from a rough slab of bone. That is, a rough piece of
not, however, report the histological type of bone
cortical bone would most profitably yield all 30”
or give standard ‘deviations. Our mean values for
specimens or all transverse specimens. Thus,
bovine Haversian femoral compact bone were:
specimens of a given orientation would be taken
from a specific portion of the bone, and the
n
question of the different properties of different
E’ = 22.6 x 10’ N/m* 8
portions of bones may play a role in producing the
E = 10.2 x 10’ N/m* 13 unexpected property variation with respect to
404 D. T. REILLY et al.

orientation. Better correspondence with predicted Also, we would like to thank Marc Martens, M.D., of
values is seen in those cases where groups of bones the Catholic University of Louvain.
are used for the different orientation specimens and
probably better sampling is had of different cortical REFERENCES
positions and their moduli. The maximal stiffness Burstein, A. H., Currey, J. D., Frankel, V. H. and Reilly,
found in those two cases for the 30” direction are D. T. (1973) The ultimate prop&ties of bone tissue: the
not impossible theoretically since an appropriate effects of yielding. J. Biomechanics 5, 35-44.
Burstein, A. H. and Frankel, V. H. (1971) A standard test
variation in the five elastic constants may predict for laboratory animal bone, J. Biomechanics 4,
this value. 1.55-1.58.
Using the constants determined in this investiga- Burstein, A. H., Reilly, D. T. and Frankel, V. H. (1973)
tion, an experimentor can then model a three Failure characteristics of bone and bone tissue.
Perspectives in Biomedical Engineering (Edited by
dimensional structure of cortical bone (plate, Kenedi, R. M.). University Park Press, Baltimore,
cylinder or shell) under complex loading configura- Maryland.
tions and predict load-deformation characteristics Hankinson (1921) Investigation of crushing strength of
in the elastic range. spruce at varying angles of grain. U.S. Air Service
Information Circular No. 259.
The overall values for the ultimate strengths of
Lang, S. B. (1970) Ultrasonic method for measuring
the human bone specimens are listed below: elastic coefficients of bone and results on fresh and
dried bovine bone. IEE, Trans. Bio. Engr 101-105,
Longitudinal Tension (+“I~
= 133 x 10”N/m2 April.
McElhaney, J. H. and Byars, E. F. (1965) Dynamic
Compression u.1, = 193 x 10” N/m2 response of biological materials. ASME 65-WA/HUF-
9.
Transverse Tension cult = 5 1 x lo6 N/m* Nadai, A. (1950) Theory of Flow and Fracture of Solids,
Vol. 1. McGraw-Hill, New York.
Compression uult = 133 X lo6 N/m* Pope, M. H. and Outwater, J. 0. (1974) Mechanical
properties of bone as a function of position and
Torsion rma. = 68 x IO”N/m*.
orientation, J. Biomechanics 7, 61-66.
(axis in Reilly, D. T. and Burstein, A. H. (1974a) The mechanical
x-direction) properties of bone tissue: A review. J. Bone ht. Surg.
56-A, 4.
These values are associated with a standard Reilly, D. T., Burstein, A. H. and Frankel, V. H. j1974b)
The elastic modulus for bone. J. Biomechanics 7,
deviation of approx. 7-10% for the ultimate normal 271-275.
stresses and 5% for the shear stresses. All of the Wang, C. (1953) Applied Elasticity. McGraw-Hill, New
above data are given with no consideration to the York.
age of the donor bone or the site of provenance of Weiss, V. (1960) Current views and theories on fracture,
crack initiation and propagation., 7th Sagamore
the specimen. They are averages of specimens from
Ordnance Materials Research Conference.
a population over the age span of 19-80yr.
The failure loads predicted with the Hankinson NOMENCLATURE
type formulation although in excellent agreement elastic modulus in isotropic plane
with experimental values, represent a first step in elastic modulus perpendicular to isotropic plane
off-axis elastic modulus
the development of a failure criteria for cortical independent shear modulus
bone polar moment of inertia
Bone tissue may be regarded as a plastic elongation at fracture
material (3.1% elongation) in its longitudinal load sustained at fracture
strain hardening modulus
direction, but does not exhibit this behavior in its off-axis ultimate stress
transverse direction (0.7% elongation). torque
ultimate strain
Acknowledgement-The authors thank the Tissue Bank in Poisson’s ratio in isotropic plane
NMRI National Naval Medical Center, Bethesda, Mary- second independent Poisson’s ration (see text)
land, for their cooperation and effort in obtaining ultimate stress
specimens for this study. In particular, we thank Robert yield stress
W. Bright, LCDR, MC, USNR, for his effort and ultimate shear stress
assistance. angle of twist per unit length.
 The elastic and ultimate properties of compact bone tissue 405

APPENDIX

HUMANFF.MUR

E@ Oult
n (x10yN/m2) (x106N/m2) EUlt
Tension
Case I L 12 17.9(3.92) 128(13.1) .023(.006

3o" 9 14.3(2.08) 95(11.6) .014(.003

60' 5 10.5(1.48) 49( 3.7) .006(.002:

T lO.l(Z.35) 50( 1.0) .008(.0011

case II L 12 18.3(4.57) 133(18.6) .032).0073

30° 4 13.2(3.65) 107( 4.0) .031(.0104

60' 4 14.9(2.80) 80( 5.2) .009(.0014

T 7 14.1(3.31) 59( 6.6) .007(.0019)

case III L 5 15.6(2.74) 133122.4) .026(.0071)

3o" 5 18.7(7.83) 105( 3.4) .021(.0064)

60' 5 15.1(2.54) 62( 5.7) .007(.0030)

T 6 13.2(2.87) 57( 3.6) .007(0015)

case IV L 6 17.9(3.22) 137(11.6) .030(.0059)

30D 5 21.9(4.93) lOO(12.9) .020(.0059)

60' 5 13.3(3.20) 55( 4.5) .006(.0008)

T 5 13.4(3.34) 62( 8.9) .007(.0016)

Compression

case v L 13 18.2(0.85) 187(28.8) .026(.0004)

30° 5 14.6(0.67) 173(13.8) .028(.0052)

60' 7 11.3(0.94) 133(15.0) .031(.0010)

T 5 11.7(1.01) 132(11.4) .028(.0029)

BOVINE HAVERSIAN FEMUR

Em OuLt
n (x10yN/m2) (x106N/m2) EUlt
Tension
Case VI L 3 23.1(3.18) 144( 6.2) .016(.0048)
3o" 4 16.7(4.54) 90( 7.5) .011(.0036)
60' 6 12.8(1.57) 60( 4.1) .008(.0014)
T 5 10.4(1.64) 46( 7.1) .009(.0011)
Compression

Case VII L 5 22.3(4.62) 254(25.5) .016(.0015)

3o" 14 15.1(1.50) lqO(12.6) .025(.0038)
60' 2 10.6(0.23) 148( 2.6) .032(.0006)
T 4 lO.l(l.78) 146(21.8) .031(.0016)
BOVINE LAMINAR FEMUR

Tensioll
Case VIII L 6 26.5(5.37) L67( 8.8) .033(.0049)
3o" 17, 18.0(1.69) lll( 7.9) .012(.0023)
60' 6 15.2(1.90) 68(12.6) .007(.0023)
T 25 lL.O(l.73) 52( 7.7) .007(.0012)
BOVINE HAVERSIAN FEMUR, Tension in Isotropic Plane
Case IX E OUlt
n (x10yN/m2) (x106N/m2) 'ult Y

Transverse (y) 4 13.0(4.62) 54(5.8) .007(.0042) .45(.250)

3o" 7 11.3(3.19) 53(8.7) .009(.0034) .47(.106)
60° 4 10.6(1.69) 49(9.1) .008(.0043) .34(.071)
Radial (z) 6 10.0(0.50) 39(4.7) .007(.0018) .44(.040)