Bone Vol. 23, No.

1
July 1998:6772

Changes in the Fracture Toughness of Bone May Not Be

Reflected in Its Mineral Density, Porosity, and
Tensile Properties
X. D. WANG,1 N. S. MASILAMANI,1 J. D. MABREY,1 M. E. ALDER,2 and C. M. AGRAWAL1
1

Department of Orthopaedics and 2Department of Dental Diagnostic Science, The University of Texas Health Science Center at San Antonio,
San Antonio, TX, USA

Introduction
Age-related changes in the skeleton often lead to an increase
in the susceptibility of bone to fracture. Such changes most
likely occur in the constituents of bone, namely, the mineral
and organic phases, and in their spatial arrangement manifested as orientation and microstructure. In the past, however, bone loss or decline in bone mineral density has been
considered to be the major contributing factor for the increased risk of bone fractures, and elastic modulus and
ultimate strength have been commonly used to assess bone
quality and strength. However, whether these properties
provide sufficient information regarding the likelihood of
bone to fracture remains debatable. Using a novel fracture
toughness test, which measures the energy or stress intensity
required to propagate a crack within a material, the objective
of this study was to investigate if the mineral density and
mechanical properties of bone can accurately predict bone
fragility as measured by fracture toughness. Changes in
fracture toughness (KIC), bone mineral density (BMD), elastic modulus (E), yield and ultimate strength (sy and ss),
porosity (P0), and microhardness (Hv) of bone were examined
as a function of age in a baboon model. With increasing age,
the fracture toughness of bone decreased, and its microhardness increased. However, no significant changes were found
in BMD, E, P0, sy, and ss as a function of age. In addition,
simple regression analyses revealed no significant correlation
between bone fracture toughness and the other parameters,
except for microhardness of bone. The results of this study
indicate that changes in bone fracture toughness may not be
necessarily reflected in its mineral density, porosity, elastic
modulus, yield strength, and ultimate strength. (Bone 23:
6772; 1998) 1998 by Elsevier Science Inc. All rights
reserved.

Age-related changes in the skeleton may lead to an increase in

the susceptibility of bone to fracture.22 Such changes most likely
occur in the constituents of bone, namely, the mineral and
organic phases, and in their spatial arrangements, such as orientation and microstructure.15,23 Although decreased bone mineral
density (BMD) has been shown to be a major contributing factor
of fracture risk,9,12 the roles of other factors, such as bone
microstructure and organic phase, are still not well understood.
Some studies have investigated effects of these factors on bone
fracture properties.3,16,18,28,29,33,34 For instance, a study by McCalden and coworkers indicated that even without significant
changes in bone mineral density, the tensile strength of bone can
decrease with age due to increased porosity.18 Similarly, Yeni et
al. showed that the fracture toughness of bone significantly
changed with bone porosity, but had no correlation with mineral
content.33,34 On the other hand, some studies have demonstrated
that the fracture toughness is correlated with bone density.3,32
Moreover, studies have also reported that variations in bone
microstructure and osteon morphology result in significant
changes in bone fracture toughness.28,34 As far as the organic
phase is concerned, Kovach and colleagues found that changes in
structural characteristics of collagen network detected using a
laser fluorescence technique significantly correlated with bone
fracture toughness.16 In a recent study conducted by Wang et al.,
collagen denaturation was found to correlate significantly with
the fracture toughness of bone,29 showing that besides bone
mineral density, porosity, and bone microstructure, changes in
the collagen network can also lead to significant variations in
bone fracture properties. All these results suggest that bone
fracture properties are determined by multiple factors.
In the past, elastic modulus and ultimate strength have been
commonly used to assess bone quality and strength.18,21 However, whether these properties can provide sufficient information
regarding the likelihood of bone to fracture is still debatable.
Because in vivo bone fractures are often initiated and/or promoted by cracks,27 fracture toughness, a measure of the energy
or stress intensity required to propagate a crack within a material,
may provide a more meaningful assessment of the susceptibility
of bone to fracture. Based on this consideration, researchers have
started to investigate bone fracture behavior using various fracture mechanics approaches. Although bone is neither homogeneous nor isotropic, Norman et al. demonstrated that linear
elastic fracture mechanics approaches are still valid for assessing
the fracture toughness of bone as long as the same type of bone

Key Words: Bone; Bone mineral density; Fracture toughness;

Tensile properties; Microhardness; Porosity.

Address for correspondence and reprints: Xiaodu Wang, Ph.D., Orthopaedic Bioengineering, The University of Texas Health Science Center,
7703 Floyd Curl Drive, San Antonio, TX 78284-7774. E-mail:
wangx@uthscsa.edu
1998 by Elsevier Science Inc.
All rights reserved.

67

8756-3282/98/$19.00
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X. D. Wang et al.
Fracture toughness vs. BMD, porosity, and tensile property

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July 1998:6772

is compared.20 Besides mode I fracture toughness,5,20 some

recent studies also investigated mode II (shear) and mode III
(tear) fracture toughness of bone.13,19 However, most of these
techniques are only suitable for testing large bone specimens
from large species such as bovine. This drawback has strictly
limited the use of well controlled animal models in studying bone
fracture properties. To alleviate this problem, a novel sandwich
technique has been recently developed to allow for testing of
bone specimens from animals as small as rabbits.30
The hypothesis of the present study is that the measurements
of bone mineral density, porosity, and tensile properties alone do
not necessarily reflect changes in the fracture toughness of bone.
Using the sandwich technique and a baboon model, this study
was performed to investigate the correlation of bone fracture
toughness with bone mineral density, porosity, and tensile properties. Changes in fracture toughness (KIC), bone mineral density
(BMD), elastic modulus (E), yield and ultimate strength (sy and
ss), porosity (P0), and microhardness (Hv) of bone were examined as a function of age.
Materials and Methods
Femora from 18 baboons (8 males and 10 females), ranging from
6 to 26 years of age, were obtained from the Southwest Foundation for Biomedical Research, San Antonio, Texas, and fresh
frozen at 220C until testing. All animals were carefully
screened to avoid the influence of any pathologies on bone.
Baboons commonly reach skeletal maturity at approximately 6
years of age,2 and their life span is usually considered to be 20
years. To cover the age ranges of young adults, middle aged, and
the elderly, these animals were divided into three age groups:
6 9, 10 16, and over 16 years old, respectively (n 5 6 in each
group). Haversian bone was the dominant microstructure of the
baboon bone samples tested in this study. There were three males
and three females each in the young adult and elderly groups,
whereas the middle aged group was comprised of two males and
four females.
The mid-diaphysis was extracted from each femur and used
for preparing biomechanical test specimens. Before specimen
preparation, the BMD of these mid-diaphyseal samples was
measured using quantitative computed tomography (QCT). In
general, it is desirable to measure the BMD directly on the test
specimens. However, the specimen size used in this study was
too small to acquire accurate BMD measurements. To ensure that
the measured BMD values were representative of the test specimens, all measurements were made at the cross section of the
diaphysis from where the test specimens were subsequently
obtained. An area of 2 3 2 mm was used for each measurement.
A hydroxyapatite phantom with three known densities was used
to obtain a calibration curve: QCT measurements (in
hounsfields) vs. hydroxyapatite density (g/cm3). Values of BMD
were then calculated based on this calibration curve and QCT
readings.
A single-layer compact sandwich (SCS) specimen (Figure 1)
was used to estimate the mode I fracture toughness (critical stress
intensity factor, KIC), which is a measure of the resistance of a
material to crack growth.30 To fabricate this specimen, polymethylmethacrylate (PMMA) was used as the holder material.
Longitudinal bone coupons (20 3 3.5 3 2 mm) were cut and
machined from the lateral aspect of each femoral diaphysis. The
bonding surfaces of the coupons were first cleaned and dehydrated by acetone and dried for 5 sec using pressurized air. The
coupons were then carefully cemented between two PMMA
holders using a cyanoacrylate adhesive (Quicktite, Loctite
Corp., Rocky Hill, CT). As shown in Figure 1, a starter notch was
cut in the middle of the bone interlayer using a circular saw and

Figure 1. Configuration of an SCS specimen for bone fracture toughness

tests. A bone coupon was sandwiched between two holders and a notch
with a precrack at its end was introduced in the middle of the bone layer.
The specimen was loaded until the crack propagated through the bone
layer. The key dimensions of the specimen were W 5 17.5 mm, B 5 3.5
mm, h 5 2 mm, and a 5 7.5 mm.

then a precrack was introduced using a sharp razor blade. The

specimens were kept moist throughout the preparation and testing process, which followed a procedure previously described.28
In this study, only longitudinal fracture toughness was measured
due to lack of bone stock for preparing test specimens in other
orientations. It has been demonstrated that bone fracture toughness alters with respect to crack orientations, and the longitudinal
direction is the weakest orientation in bone.4,6
The E, sy, and ss of bone were determined using a tensile
test. Flat dumb-bell shaped tensile test specimens were extracted
from the lateral aspect of the same mid-diaphysis used for the
fracture toughness test specimens. Because the bone stock at the
lateral aspect was limited, the size of the tensile specimens was
determined by the available bone volume remaining after the
fracture toughness test specimens were taken. The overall length,
gage length, gage width, and gage thickness of the specimens
were 30, 10, 2, and 1 mm, respectively. These specimens were
loaded to failure in tension in an Instron machine at a constant
loading speed (3 mm/min), and the resulting load-displacement
curve was used to calculate the elastic modulus and tensile
strength of bone.
The measurements of porosity were performed on a cross
section of the diaphysis adjacent to the site from where the
biomechanical test specimens were taken. The cross section was
embedded in a plastic resin and polished following standard
procedures for engineering materials. Thereafter, an image of the
cross section was digitized into a computer via a light microscope. Then an image processing and computational code written
in the National Institutes of Health (NIH) Image macro programming language was used to calculate the ratio of the area of
cavities (Haversian and vascular canals) with respect to the
whole area of the image. This ratio was defined as the porosity
of bone.
Vickers microhardness was measured using a microhardness
tester (Micromet, Adolph I. Buehler, Inc., Evanston, IL) on the
same cross section utilized for measuring porosity. To be consistent, microhardness was measured only in the interstitial
regions. An average microhardness value was obtained from

Bone Vol. 23, No. 1

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X. D. Wang et al.
Fracture toughness vs. BMD, porosity, and tensile property

69

Table 1. Summary of experimental data (n 5 6)

Age (years)

KIC
(MPaum)

E (GPa)

ss (MPa)

sy (MPa)

dm (g/cm3)

Hv (kg/mm2)

P0 (%)

610
1116
.16
ANOVA

2.25 6 .18
2.28 6 .29
1.73 6 .25
p , 0.002

4.55 6 1.82
4.89 6 0.80
5.03 6 1.47
p . 0.8

180 6 26.6
164 6 12.1
190 6 14.2
p . 0.09

147 6 3.4
139 6 11.6
154 6 15.5
p . 0.18

1.33 6 0.01
1.29 6 0.01
1.35 6 0.02
p . 0.2

48.9 6 4.1
51.3 6 5.2
60.5 6 10.2
p , 0.03

3.3 6 1.2
3.6 6 1.3
5.4 6 2.8
p . 0.3

Differences are significant only when p , 0.05. KIC: mode I fracture toughness; E: elastic modulus; ss: ultimate strength; sy: yield strength; dm: bone
mineral density measured using QCT; Hv: Vickers microhardness; and P0: porosity measured on the cross section of femora using an image processing
technique.

three measurements at randomly selected locations on each

sample.
All experimental data were compiled as mean and standard
deviation (mean 6 SD). A one-way analysis of variance
(ANOVA) was employed to detect differences in all measured
parameters as a function of age. The parameters indicating
significant changes with age were considered to be the agedependent parameters, and a simple regression analysis was
utilized to explore the correlation between the measured
parameters.

toughness, increased sharply for the elderly group as shown in

Figure 3.
No statistically significant differences were found in E, BMD,
sy, ss, and P0 between the three age groups (p . 0.05).
Simple regression analyses showed that no significant correlation existed between BMD, porosity, tensile properties, and
fracture toughness of bone (p . 0.05). However, the regression
analysis indicated that the fracture toughness decreased with
increasing microhardness (Figure 4), although there was only a
relatively weak correlation between the two (p 5 0.077).

Results

Discussion

The experimental results are summarized in Table 1. Although

the fracture toughness changed significantly as a function of age
(p , 0.05), no significant difference was observed between the
young adult and middle-aged group (6 10 and 1116 years,
respectively). The mean fracture toughness values for these two
age groups were similar to that (2.17 6 0.27 MPaum) obtained
in a previous study.31 However, the fracture toughness sharply
dropped for the elderly group (.16 years) as shown in Figure 2.
The microhardness of bone (Hv) was another parameter that
changed significantly with age (p , 0.05). In the ANOVA
analysis, the microhardness showed no significant changes for
young adult and middle-aged groups, but in contrast to fracture

To evaluate the biomechanical competence of bone, two basic

aspects have to be taken into account: morphometric and material
properties. Morphometric properties provide information pertaining to the size, shape, and other structural characteristics of
bone, while material properties are representative of its intrinsic
mechanical properties. The strength of any given bone relies on
both these properties, and age-related changes in bone may occur
exclusively in either of them or simultaneously in both. In this
study, only the material properties of baboon cortical bone were
examined as a function of age. Among the parameters measured,

Figure 2. Fracture toughness of bone as a function of age. Mode I

longitudinal fracture toughness (KIC) was measured using a single-layer
sandwich specimen. A significant decrease in KIC was found for the
elderly compared to younger groups (p , 0.05).

Figure 3. Microhardness of bone as a function of age. The microhardness (Hv) of the interstitial regions was measured on the cross section of
each femoral diaphysis using a Vickers microhardness tester. A significant increase in Hv was found for the elderly compared to younger groups
(p , 0.05).

70

X. D. Wang et al.
Fracture toughness vs. BMD, porosity, and tensile property

Figure 4. Correlation of the fracture toughness of bone with its microhardness. A relatively weak correlation (p 5 0.077) was found between
the two parameters in a simple regression analysis. The dotted line
depicts the linear regression of the data (r2 5 0.26).

age-related changes were detected only in the fracture toughness

and interstitial microhardness of bone, while the BMD, porosity,
and tensile properties exhibited no significant changes. These
results indicate that: (1) the fracture toughness of bone decreases
with age; (2) bone fracture toughness varies even though no
changes occur in its BMD, porosity, and tensile properties; and
(3) besides BMD and porosity, other factors may be responsible
for the decreased fracture toughness of bone.
Baboon bone samples tested in this study exhibited no significant changes in both porosity and BMD with increasing age,
which is not in good agreement with the results obtained from
human cortical bone in the literature.18,33,34 This is probably due
to the differences between the two species. For instance, the
porosity value of baboon cortical bone obtained in this study
varied between 3% and 8%, which is extremely small compared
to reported values (between 5% and 30%) of human cortical
bone.18,34 Given this small range, normal limitations associated
with data measurements, and other non-age-related differences
between the specimens, it is quite likely that tests in the present
study were unable to detect age-related changes in the porosity of
baboon bone. A further, more detailed, study with a large number
of specimens will be required to explore this issue. However, it
should be pointed out that the intent of the present study was to
investigate the correlation of fracture toughness of bone with its
mineral density, porosity, and tensile properties. Although agerelated changes in baboon bone may not closely mimic similar
changes in human bone, it is unlikely that this difference would
significantly influence the correlation between bone properties.
It is noteworthy that in the present study the mean elastic
modulus values were within the range of 4.555.03 GPa for the
different age groups, and were much smaller compared to the
value (15.4 GPa) obtained in a three-point bending test in a
previous study.31 This is probably due to the effects of a small
specimen size. It has been found that a small specimen size can
lead to decreased bone stiffness values due to the weakening
effects of osteons.10 In addition, all testing systems have an
inherent error caused by system deformation and play in their

Bone Vol. 23, No. 1

July 1998:6772

moving parts. Such errors can lead to an underestimation of

elastic modulus if the deformation of test specimens is very small
and of the same order of magnitude as the errors. However, such
errors would be expected to have little influence on detecting
relative differences between the specimens as long as the specimen size and test condition are consistent. Moreover, due to the
restrictions imposed by limited bone stock and the test methodologies used, the failure planes in fracture toughness and tensile
tests were different. In the fracture toughness test, cracks travel
in a longitudinal plane, whereas in the tensile test failure occurs
at the transverse plane of the femoral diaphysis. Thus, these two
tests would reflect age-related changes in bone at different
orientations. Finally, it should be pointed out that due to limited
specimen sizes the measurements of BMD, porosity, and microhardness were not performed directly on the biomechanical test
specimens. However, since all these measurements were performed at a similar anatomical location, the values obtained
would be expected to be representative of the test specimens.
Baboon bone samples tested in this study exhibited no significant changes in both porosity and BMD with increasing age,
which is not in agreement with the results obtained from human
cortical bone in the literature.18,33,34 This is probably due to the
discrepancy between the two species. For instance, the porosity
value of baboon cortical bone obtained in this study varied in a
range between 3% and 8%, which is extremely small compared
to that (between 5% and 30%) of human cortical bone reported
in the literature.18,34 Considering non-age-related differences
between the samples and errors associated with the measurement,
it is possible that the sample size used in this study was too small
to detect age-related changes in such a small range (a few
percent) for the baboon bone samples tested. However, it should
be pointed out that the intent in the present study was to
investigate the correlation of the fracture toughness of bone with
its mineral density, porosity, and tensile properties. Although
age-related changes in baboon bone may be more or less different from humans, it is unlikely that such a discrepancy may cause
misleading conclusions to be made when the correlation between
the bone properties is explored in this baboon model.
Age-related changes in the longitudinal fracture toughness of
bone have been reported by several investigators.6,8,19 The results of their studies on human bone indicated that the fracture
toughness of bone decreased with age for both genders. The
results of our study exhibited the same trend in baboon bone,
suggesting that bone becomes more susceptible to crack growth
with increasing age.
In the present study, the BMD measured is actually an
apparent mineral density, which represents the amount of mineral
in a unit volume of bone. Thus, its value is primarily influenced
by two factors: true mineral density and porosity. No significant
age-related changes were found in both BMD and porosity in this
study, thereby indicating no significant changes in the true
mineral density as well. Because elastic modulus of bone is
determined primarily by bone mineral content (or true density),11,17,25 similar elastic modulus values would be expected for
all age groups tested. This result is in agreement with reports on
human bone by McCalden et al.18 and Yeni et al.33 Moreover, the
results of our study indicate that the ultimate strength was
relatively constant over the different ages. Considering the fact
that there was little variation in BMD and porosity in the bone
specimens tested (Table 1), no significant changes in bone
strength would be expected because the ultimate strength of bone
is primarily determined by these factors.18,26 However, the fracture toughness of these bone specimens changed significantly,
suggesting that the ultimate strength of bone may not adequately
reflect its fracture toughness. This is not surprising because these
two parameters describe different aspects of the biomechanical

Bone Vol. 23, No. 1

July 1998:6772

behavior of bone; fracture toughness measures the ability of a

material to resist fractures associated with crack propagation,1
while the ultimate strength does not take cracks into account.
Additionally, these two tests actually reflect bone fracture properties in different orientations (e.g., longitudinal and transverse).
Because bone is anisotropic in nature, bone fracture properties
may vary significantly in different orientations.4,28 In a recent
study, Zioupos and Currey reported that the transverse fracture
toughness of human cortical bone had a strong correlation with
the stiffness and strength obtained in the same orientation.35
Thus, the correlation between bone fracture properties is orientation dependent.
Bone is a composite material comprising mineral and organic
phases.7,14 Changes in any of these components and their spatial
arrangement may contribute to the fracture toughness of bone.
Among the relevant parameters, bone density has been reported
to be significantly correlated with mode I (tension) fracture
toughness of bone.6,32 Similarly, Yeni et al. reported that the
mode I fracture toughness of human femora significantly correlated with bone density, but exhibited little correlation with bone
mineral content.33 In another study, Yeni et al. found that bone
fracture toughness decreased with increasing porosity as a function of age.34 In the present study, the fracture toughness of
baboon bone showed significant changes irrespective of relatively constant BMD and porosity. These results suggest that
bone fracture toughness may be affected not only by mineral
density and porosity but by some other factors as well. In some
recent studies relevant to this issue, it was determined that the
integrity of the collagen network (90% of organic phase of bone)
also plays a role in determining bone fracture properties.16,29
Also it was reported that bone fracture toughness had a significant correlation with osteon morphology (e.g., size, area, and
density, etc.).34 Thus, it is possible that without significant
changes in bone mineral phase and porosity, bone fracture
toughness can change due to the variation in osteon morphology
and the organic phase.
In general, microhardness is a material property that reflects
a combination of the elastic modulus (E) and yield strength
(sy).24 The linear regression analyses, however, did not show
significant correlation between interstitial microhardness and
elastic modulus or yield strength of bone for the animals tested
(p . 0.05). In this study, we only measured interstitial microhardness. Because Haversian systems also play a role in determining bone mechanical properties, it is possible that an increase
in the interstitial microhardness may not lead to significant
changes in mechanical properties of the entire tissue. Moreover,
although both the microhardness and fracture toughness of bone
changed as a function of age, there was only a relatively weak
correlation between the interstitial microhardness and fracture
toughness of bone (p 5 0.077). Because the measured microhardness only reflects material properties of interstitial region, a
stronger correlation may become obvious if the influence of
Haversian systems is taken into consideration. The underlying
mechanisms for the relationship between fracture toughness and
microhardness are not clear and further studies are needed to
address this issue.
In summary, the results of this study indicate that interstitial
microhardness and longitudinal fracture toughness of baboon
bone significantly change with age. However, these changes are
not reflected in the elastic modulus and tensile strength and are
independent from the apparent bone mineral density and porosity. This suggests that apparent mineral density, porosity, and
tensile properties alone do not always reflect changes in the
fracture toughness of bone.

X. D. Wang et al.
Fracture toughness vs. BMD, porosity, and tensile property

71

Acknowledgments: Special thanks are due to Dr. G. B. Hubbert, S.

McAnn, and M. Silva, Southwest Foundation for Biomedical Science,
San Antonio, TX, for providing the baboon tissue.

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Date Received: September 18, 1997

Date Revised: March 30, 1998
Date Accepted: March 31, 1998